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Neuropsychologia 50 (2012) 1054– 1071

Contents lists available at SciVerse ScienceDirect

Neuropsychologia

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motional processing and its impact on unilateral neglect and extinction

udith Domínguez-Borràsa,∗, Arnaud Saja,b, Jorge L. Armonyc, Patrik Vuilleumiera,b

Laboratory for Behavioral Neurology and Imaging of Cognition, Department of Neuroscience, University Medical Center, 1 rue Michel-Servet, 1211 Geneva, SwitzerlandDepartment of Neurology, University Hospital, 1 rue Michel-Servet, 1211 Geneva, SwitzerlandDepartment of Psychiatry, McGill University, Douglas Institute, Research Pavilion Frank B. Common Rm. F-1146 6875, LaSalle Blvd., Montreal, Quebec, Canada

r t i c l e i n f o

rticle history:eceived 15 November 2011eceived in revised form 29 February 2012ccepted 1 March 2012vailable online 8 March 2012

eywords:motionttentionnilateral spatial neglectxtinction

a b s t r a c t

Unilateral spatial neglect is a neurological disorder characterized by impaired orienting of attentionto stimuli located in the contralesional space, typically following right-hemisphere damage. Neuropsy-chological investigations in the past two decades have demonstrated that neglect is caused by deficitsaffecting a widespread cortico-subcortical fronto-parietal network controlling spatial attention, but usu-ally sparing early sensory pathways. As a consequence, certain residual abilities in sensory processingremain intact and still take place for stimuli in the neglected space, such as the extraction and organiza-tion of coherent or meaningful object features. Moreover, these residual abilities can alleviate inattentionsymptoms when contralesional stimuli are perceptually or biologically salient. Here we review recentstudies suggesting that the emotional content of stimuli may also be processed despite impaired attentiontowards contralesional space, and that such processing may act to enhance attention and partly reduceneglect for these stimuli, relative to similar but emotionally neutral stimuli. For example, faces withemotional expressions, voices with emotional prosody, as well as pictures of scenes or even spiders havebeen found to be less severely extinguished from awareness in conditions of bilateral stimulations, and/orlead to fewer omissions in search tasks with multiple distracters. Gaze cues and reward learning mightalso produce similar effects. Altogether, these findings suggest that emotionally significant informationis not only extracted from stimuli at neglected locations through spared pathways, but can also induceemotional biases in attention that partly counteract the abnormal spatial biases caused by fronto-parietaldamage. We discuss results from neuropsychology and neuroimaging research suggesting that specific

mechanisms for emotional attention might exist, centered on the amygdala and other limbic regions,and that these mechanisms can operate partly independent from other circuits controlling spatial andobject-based attention. Although we are only beginning to understand these interactive effects of emo-tion and attention and to identify their neuroanatomical substrates, we believe that a deeper knowledgeof such mechanisms and their conditions of optimal operation will help develop or improve therapeutic strategies in neglect patients.

© 2012 Elsevier Ltd. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10552. Rescue from spatial neglect by low-level saliency effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10563. Effects of emotional saliency on spatial neglect and extinction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10574. Neural substrates of attention and impaired awareness in spatial neglect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10615. Neural substrates for emotional influences on attention and spatial neglect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10626. Preattentive pathways to the amygdala . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10657. Other modulations of spatial neglect by affective, motivational or social factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1066

8. Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author. Tel.: +41 22 37 95361; fax: +41 022 379 5402.E-mail address: Judith.dominguezborras@unige.ch (J. Domínguez-Borràs).

028-3932/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2012.03.003

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. Introduction

Unilateral spatial neglect (USN) is defined by a failure to detect,espond to, and act on stimuli located in the space contralateral to

focal brain lesion (Driver, Vuilleumier, & Husain, 2004; Heilman,atson, & Valenstein, 1985; Vuilleumier, 2007). Patients may shave

r put make up only to the ipsilesional half of their face, answernly when addressed from the ipsilesional side while ignoringtimulation from the contralesional side, and/or fail to turn theiraze and move their limbs towards a contralesional stimulus. Thistriking disorder is usually conceived as resulting from a loss inhe contralesional representation of space or in the orientation ofttention towards the contralesional side of space. Specifically,eglect symptoms are misses in contralesional stimuli presentedlone, whereas extinction symptoms appear when a patient suc-essfully responds to single contralesional stimuli, but misses thoseresented together with stimuli on the ipsilesional space. Such loss

n the contralesional space does not appear to be fixed: neglectehavior may vary in the same patient when tested in differentccasions or in different tasks, indicating that the mentioned spaceepresentation and/or control of spatial attention reflect dynamicrocesses that are subject to modulations by various other factors.ence, even though patients with unilateral spatial neglect typ-

cally behave as if the contralesional side of space did not exist,any instances show that some part of it or some information in

t may still be processed and represented in their brain (Driver &uilleumier, 2001a, 2001b). USN is different to other neurologi-al deficits, such as hemiplegia or blindness, which persist in aelatively constant manner across testing occasions except for someeflexive behaviors mediated by specific pathways (e.g. movementsf the paralyzed hemibody during yawning).

USN, in its most severe and persisting form, usually occurs uponxtensive right hemisphere damage and therefore affects the leftide of space. Importantly, USN cannot be explained by primaryensory or motor deficits. A number of studies have investigatedhe brain areas most typically implicated in USN, by using var-ous clinical-anatomical correlation approaches in large patientamples, but the exact neural substrates underlying the variouseglect symptoms are still subject of hot debate (Halligan, Fink,arshall, & Vallar, 2003; Karnath & Rorden, 2011; Saj, Verdon,ocat, & Vuilleumier, 2011). USN is the most consistently encoun-

ered upon lesions to the right posterior parietal lobe, centeredn its inferior part, encompassing the angular and supramarginalyri at the temporoparietal junction (Mort et al., 2003; Vallar

Perani, 1986). However, recent studies using the technique ofoxel-based lesion-symptom mapping also found frequent damageo other cortical regions, including the posterior part of the supe-ior temporal gyrus (STG; see Karnath, Fruhmann Berger, Kuker,

Rorden, 2004; Karnath, Rennig, Johannsen, & Rorden, 2011; Sajt al., 2011), the parahippocampal region (Cals, Devuyst, Afsar,arapanayiotides, & Bogousslavsky, 2002; Doricchi & Angelelli,999; Mort et al., 2003), or the right frontal lobe, predominantlyhen affecting the inferior frontal cortex (Husain & Kennard, 1996,

997). Systematic voxel-based mapping studies have also shownhat different lesions within the right hemisphere might lead toifferent manifestations of spatial neglect. For example, deficits

n tasks involving exploratory motor components, or resistanceo distraction, are associated with lesions in the prefrontal andremotor cortex; deficits in tasks requiring more perceptual andisuo-motor transformations correlate with parietal lesions, andeficits affecting object-based coding of space correlate with tem-oral lobe damage (e.g. see Hillis et al., 2005; Verdon, Schwartz,

ovblad, Hauert, & Vuilleumier, 2010). Similar anatomical distinc-ions have been shown for other neglect symptoms (Committerit al., 2007; Rorden, Fruhmann Berger, & Karnath, 2006). In addi-ion, USN may arise from lesions restricted to either basal ganglia

chologia 50 (2012) 1054– 1071 1055

(e.g. Damasio, Damasio, & Chui, 1980; Karnath et al., 2005) or thethalamus (e.g. Kumral, Kocaer, Ertubey, & Kumral, 1995; Leibovitchet al., 1998; Rafal & Posner, 1987), in particular the pulvinar.Finally, several recent studies have emphasized the important roleof disconnections affecting the subcortical parieto-frontal (Doricchi& Tomaiuolo, 2003; Gaffan & Hornak, 1997) or both parieto-frontal and parieto-temporal (Leibovitch et al., 1998) pathwaysin the white matter (Doricchi & Tomaiuolo, 2003; Mort et al.,2003; Verdon et al., 2010). Specifically, data from diffusion tensorimaging (DTI) highlighted a high frequency of lesions in parieto-frontal association fibers, such as the right superior longitudinalfasciculus (SLF; Doricchi & Tomaiuolo, 2003) and/or the inferiorfronto-occipital fasciculus (IFOF; Nieuwenhuys, Voogd, & Huihzen,1988; Thiebaut de Schotten et al., 2005). Both fascicule intercon-nect the inferior parietal lobule and superior temporal gyrus tothe inferior frontal gyrus (Catani, Howard, Pajevic, & Jones, 2002;Catani, Jones, & Ffytche, 2005) and are known to be larger in theright than in the left hemisphere (Thiebaut de Schotten et al.,2011).

There is no common consensus as to the exact mechanismsunderlying spatial neglect. However, it is now generally assumedthat deficits in attentional processing are central to USN (seethis special issue). Several accounts in favour of an attentionalhypothesis of USN have been forwarded in literature, and differ-ent components of attentional processing have been proposed to bedefective (e.g. see Driver et al., 2004). A classic model by Kinsbourne(1970) assumes that each hemisphere orients attention towardsthe opposite hemispace, while inhibiting the activity of the otherhemisphere. In this model, the left hemisphere is dominant sothat a unilateral right hemisphere lesion would release the lefthemispheric bias to orient attention to the right, while a focal leftlesion would only rarely be sufficient to cause a significant bias tothe left. This hemispheric balance is compatible with modulationsof neglect observed after additional lesions (Vuilleumier, Hester,Assal, & Regli, 1996) or transcranial magnetic stimulation (TMS;Koch et al., 2008). Conversely, another classic model put forwardby Heilman and colleagues (Heilman & Valenstein, 1979) assumes aright hemisphere dominance for orienting attention to both sides ofspace, such that a right hemisphere lesion will cause a severe deficitfor orienting attention to the left and a milder deficit of attentionfor right space. This pattern is, indeed, consistent with many obser-vations that neglect is not strictly contralesional (e.g. Vuilleumier& Rafal, 2000).

A more recent model by Corbetta and colleagues (Corbetta,Kincade, Lewis, Snyder, & Sapir, 2005; Corbetta & Shulman, 2002)has attempted to relate distinct attentional processes to distinctanatomical substrates and proposed to distinguish between dor-sal and ventral networks for orienting spatial attention, basedon converging evidence from functional neuroimaging studies inhumans. On one hand, a dorsal fronto-parietal system, encompass-ing superior frontal cortex, superior parietal lobe and regions alongthe intraparietal sulcus, may control the preparatory and volun-tary goal-directed selection of sensory information by attention.On the other hand, a ventral system, along the temporoparietalcortex and inferior frontal cortex, may be responsible for the detec-tion of relevant stimuli when these are salient or unexpected and,thus, mediate the interruption of the current attentional focusmaintained by the dorsal system. Both the ventral system (later-alized to the right hemisphere), and the dorsal system (bilaterallydistributed) are, according to these authors, disrupted in spatialneglect. Activation of this ventral system might be triggered by var-ious stimulus properties such as sudden onset, novelty, or intrinsic

salience.

Finally, a different anatomical model put forward by Mesulam(1981) assumes that the spatial orientation of attention relies ona distributed circuitry involving three interconnected nodes. This

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etwork includes: (1) a posterior parietal component (composedf the superior and inferior parietal lobules, the intraparietal sul-us and the medial parietal cortex) which represents locations inxternal space based on behavioral salience (rather than on phys-cal stimulus properties), and in terms of coordinates, is used forkinetic plans’, such as grasping, exploring, or foveating salienttimuli, rather than in terms of absolute spatial position; (2) arontal component (centered on the frontal eye fields, the premo-or cortex and prefrontal areas) which responds preferentially toistant visual stimuli (beyond reaching distance) and mediatingotor-exploratory aspects of attention; (3) finally, a cingulate com-

onent, which responds to the motivational relevance of the stimulir task context. In this model, each of these nodes operate indepen-ently to build a representation of space, as well as to distributettention in space, through connections, not only to subcorticaltructures (superior colliculus, pulvinar, basal ganglia), but alsoo cortical areas (premotor, dorsolateral prefrontal, orbitofrontal,nsula and parahippocampal regions). Moreover, all three mainodes in this attention network may be under further modulatory

nfluences by ascending reticular inputs that determine levels ofrousal and alertness.

The latter model is particularly interesting, as it is the only modelxplicitly linking spatial attention, as well as goal-directed behav-ors, with motivation signals mediated by areas connected with theimbic system, therefore explicitly predicting that attention mighte influenced by internal motivational factors. As we describe inhis review, there are good reasons to believe this assumption isalid, even though the exact neural circuits still partly remain unre-olved. Indeed, the severity of spatial neglect is not only modulatedy general arousal or alertness (such as a sudden loud sound, seeobertson, Mattingley, Rorden, & Driver, 1998), but also appearso be influenced by specific cues with affective significance (seeuilleumier & Driver, 2007), consistent with findings in healthyarticipants showing that attention is gated by emotional signalscross different attention tasks (Vuilleumier, 2005a). Besides anec-otal evidence that the lack of attention to contralesional spacean be partly alleviated when the patients are presented with aollar bill on the neglected side (personal communication) recentxperiments have confirmed similar effects of emotion on attentionn neglect patients, using various experimental tasks and differenttimuli, while contributing to uncover the neural substrates medi-ting cross-talks between goal-dependent control and involuntaryffective guidance of attention. Nevertheless, many aspects of theseffects remain to be fully clarified. We will now start pinpointingvidence focused on the physical salience of a stimulus.

. Rescue from spatial neglect by low-level saliency effects

As noted above, neglect involves higher-order deficits in spatialepresentations and attention mechanisms, with relative sparingf elementary sensory and motor pathways (Driver & Mattingley,998; Driver & Vuilleumier, 2001a; Rotshtein et al., 2010). There-ore, neglect deficits entail a problem of directing attention toontralesional stimuli that prevents access to awareness, ratherhan a mere degradation of early sensory processing. Although thedea of intact sensory pathways has been partly qualified by, fornstance, studies showing delayed early visual-evoked potentials toontralesional stimuli (Pitzalis, Spinelli, & Zoccolotti, 1997; Spinelli

Di Russo, 1996), similarly reduced auditory and visual evoked-otentials (Tarkka, Luukkainen-Markkula, Pitkanen, & Hamalainen,011), or lower functional magnetic resonance imaging (fMRI)

ctivation of structurally intact extrastriate visual areas (Corbettat al., 2005), there is abundant evidence that neglect patientsossess residual low-level sensory-processing abilities (Driver &uilleumier, 2001b; Vuilleumier, Armony, et al., 2002). These

chologia 50 (2012) 1054– 1071

residual processes are particularly evident in conditions with lowattention demands (e.g. Vuilleumier et al., 2008). A recent event-related potential (ERP) study demonstrated that visual responsesmay remain unaffected up to 130 ms after stimulus-onset in neglectpatients, yielding unaffected C1 and P1 scalp – ERP components tocontralesional visual stimuli (Di Russo, Aprile, Spitoni, & Spinelli,2008). Possible abnormalities would arise only after this time-point, relative to healthy individuals, or even patients with braindamage but no neglect (Di Russo et al., 2008). Other studies havecompared ERPs evoked by contralesional visual stimuli when extin-guished and when consciously perceived. These single studies,all performed in single cases, have also shown divergent resultsincluding attenuated or abolished P1 and N1 to unseen stimuli(Driver, Vuilleumier, Eimer, & Rees, 2001; Marzi, Girelli, Miniussi,Smania, & Maravita, 2000), or preserved early visual responses witha reduction or absence of later responses such as the N170/P190to faces (Vuilleumier, Armony, Driver, & Dolan, 2001) and theP300 (Lhermitte, Turell, LeBrigand, & Chain, 1985; Verleger, Heide,Butt, Wascher, & Kompf, 1996). In healthy subjects, P1 and N1components are typically enhanced by top-down attention mech-anisms, while earlier C1 activity is generally sensitive to task loadand visual learning, but not selective attention (Rauss, Pourtois,Vuilleumier, & Schwartz, 2011). Taken together, however, theseresults in neglect patients have been interpreted as reflecting pre-dominant anomalies at later perceptual stages involving feedbackprojections from higher to lower visual areas (Di Russo et al., 2008),and thus affecting attention selection and conscious awareness,while early bottom-up processes are generally intact. Accordingly,single-photon emission computed tomography (SPECT) and fMRIstudies in neglect patients also suggested that activity in early cor-tical areas (e.g. primary visual cortex – V1) might still arise forstimuli in the neglected contralesional hemifield, as compared withthe intact ipsilesional hemifield, even without conscious detec-tion (Rees et al., 2000; Vuilleumier, Sagiv, et al., 2001). In contrast,conscious detection might be accompanied by further enhance-ment in these early retinotopic areas due to re-entrant feedbacksignals from higher-level (frontal or parietal) areas, accompaniedwith additional processing at subsequent stages along the per-ceptual pathways, e.g. in object recognition areas (Vuilleumier,2005b). Similar re-entrant feedback effects have also been relatedto conscious vision in the intact brain of healthy people duringmasking paradigms (Dehaene et al., 2001; Lamme, 2003; Peyrinet al., 2010).

In fact, the existence of bottom-up processing prior to atten-tion selection is compatible with the idea that mechanisms ofexogenous orienting have evolved to direct attention to relevantstimuli, based on the ability to rapidly detect salient informationthat is potentially behaviorally relevant or crucial for survival. Thus,whereas unattended stimuli often escape awareness even in nor-mal subjects, some preattentive processing can still occur in orderto guide orienting to the most salient events, and hence lowerthe threshold for conscious perception (see Dehaene, Changeux,Naccache, Sackur, & Sergent, 2006). Such saliency can be deter-mined by different properties of the objects including their suddenonset or unexpectedness, contextual novelty, or frequency ofoccurrence (Corbetta & Shulman, 2002), but also intrinsic sensoryfeatures such as brightness, color, or size, or even long-term learnedimportance and familiarity (see Desimone & Duncan, 1995). In thissense, the notion that patients with unilateral neglect and extinc-tion often present with spared structural (and often functional)sensory pathways may help understand residual “pre-attentive”abilities. Importantly, this would account for neuropsychological

findings showing that extensive unconscious processing can stilltake place in the neglected field (Driver & Mattingley, 1998), eventhough these patients have difficulties in directing attention to thatside, both exogenously and endogenously (Ladavas, Menghini, &

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milta, 1994). However, the nature and degree of such residualrocessing might differ across individual patients due to the vary-

ng location and extent of lesions (e.g. see Vuilleumier, Valenza, &andis, 2001).

The pop out phenomenon in visual search (Treisman & Souther,985) is a classic example of processing of salient visual featuresrior to top-down, serial attention (although the pop out effect

tself requires the subsequent focusing of attention on targets (e.g.ee Cohen, Alvarez, & Nakayama, 2011). For instance, a single redot among a cloud of blue dots will be noticed almost imme-iately regardless of the number and arrangement of blue dots.his phenomenon is typically explained by bottom-up processesn visual pathways that can extract local salient discontinuities inhe visual scene and then capture attention in a reflexive manner.

number of studies using visual search tasks in neglect patientsave reported some degree of pop out when searching for tar-ets defined by color (Esterman, McGlinchey-Berroth, & Milberg,000; Kristjansson, Vuilleumier, Malhotra, Husain, & Driver, 2005;ucas & Vuilleumier, 2008) or texture (Aglioti, Smania, Barbieri, &orbetta, 1997), suggesting that these low-level processing abilitiesre preserved despite inattention, in both the ipsi- and contrale-ional visual hemifields. However, it must be noted that othertudies reported little or absent pop-out effects when manipulatingisual stimulus contrast (Smania, Martini, Prior, & Marzi, 1996), orresenting color singletons in the contralesional space (Behrmann,bert, & Black, 2004; Pavlovskaya, Ring, Groswasser, & Hochstein,002). These discrepancies remain partly unresolved but mightotentially result from different lesion extents (e.g. see Vuilleumier,alenza, et al., 2001).

Neglect and extinction can also be attenuated by early “preat-entive” operations that organize visual information in extrastriatereas across the two visual hemifields, such as defining axes orrouping of candidate objects according to Gestalt principles. Inact, in normal vision, perceptual organization and object-basedegmentation processes are generally held to occur before atten-ional search (Treisman, 1982). Accordingly, contralesional neglectfor a single stimulus) or extinction (for a stimulus accompaniedith a distractor on the opposite side) can be reduced by figure-

round segregation (Mattingley, Davis, & Driver, 1997; Vuilleumier Landis, 1998), symmetry perception (Driver, Baylis, & Rafal, 1992;ilchrist, Humphreys, & Riddoch, 1996; Ward, Goodrich, & Driver,994), grouping by illusory contours in Kanisza figures across hemi-elds (Vuilleumier, Valenza, et al., 2001) or by common shapeVuilleumier & Sagiv, 2001), and even by grouping with task-rrelevant distractors in the neglected field during the detectionf ipsilesional targets (Shomstein, Kimchi, Hammer, & Behrmann,010). Preattentive processing according to Gestalt organizationay also influence perception within one hemifield, as shown,

or instance, when the strength of grouping in left-sided stimulinhance their detection (Robertson, Eglin, & Knight, 2003). Sim-larly, extinction can be overcome when contralesional stimuliorm together existing or plausible objects, as opposed to scram-led or open shapes (Rappaport, Riddoch, & Humphreys, 2011;uilleumier, 2000; Vuilleumier & Sagiv, 2001; Ward & Goodrich,996), or when letter strings form words, in contrast to non-wordsBaylis, Driver, Baylis, & Rafal, 1994). Extinction rates also decreasehen two contralesional objects are spatially positioned such that

hey may be used together (e.g. a corkscrew that has to be insertednto the cork of a bottle (see Riddoch, Humphreys, Edwards, Baker,

Willson, 2003). Finally, attention is biased towards good, mean-ngful objects over meaningless stimuli (Ward & Goodrich, 1996),

hose categorization is presumably mediated by early, bottom-

p processing in the occipitotemporal visual pathways (Berti &izzolatti, 1992; Di Russo et al., 2008; Hirsch et al., 1995; Lucas

Vuilleumier, 2008; Vuilleumier & Schwartz, 2001b; Vuilleumier,alenza, et al., 2001).

chologia 50 (2012) 1054– 1071 1057

All these findings provide evidence that attentional deficitsin neglect and extinction patients often spare the ability to dis-criminate between the most purposeful and relevant objects overnon-purposeful or non-relevant stimuli, suggesting that substan-tial stimulus analysis may still take place in intact sensory areaswithout attention. These effects do not only involve simple pop-out physical features, but also more global stimulus structure andobject-based organization processes. Taken together, such find-ings indicate that perceptual analysis and competition for attentioncan be biased in favor of a subset of stimuli based on the “pre-paredness” of some neural circuits to encode and respond to thesestimuli, insofar as these circuits can be recruited without top-downattention. Besides these effects of low-level visual features andGestalt organization, recent studies also suggest that emotionalinformation might be extracted from unattended stimuli throughspared pathways and contribute to capture attention more readilythan emotionally neutral events. As we will discuss next, we areonly beginning to understand these effects and identify their neu-roanatomical substrates.

3. Effects of emotional saliency on spatial neglect andextinction

As mentioned above, the saliency and meaningfulness of astimulus can facilitate its conscious perception by increasing itsweight in the competition for attention, an effect observed in bothhealthy subjects and patients with spatial neglect (see Vuilleumier,2005a). An example of such facilitation for behaviorally andaffectively meaningful stimuli is provided by face processing. Facesare special objects with particular biological and social signifi-cance, perhaps associated with some innate (or at least overlearnt)salience (Johnson, 2011). Accordingly, even in healthy people, faceshave been found to be more likely perceived under conditionsof inattention, or divided attention, relative to other categoriesof stimuli (Bindemann, Burton, Hooge, Jenkins, & de Haan, 2005;Langton, Law, Burton, & Schweinberger, 2008; Mack & Rock, 1998).Likewise, one study (Vuilleumier, 2000) reported that patientswith left spatial neglect showed less extinction towards neutralfaces presented contralesionally in bilateral displays (i.e. with aconcurrent ipsilesional distractor), as compared to when the con-tralesional stimuli were meaningless shapes, written names, oreven scrambled faces. Conversely, bilateral displays led to greaterextinction of contralesional shapes when the concurrent rightstimuli were faces. Strikingly, in some trials, faces presented onthe left (and therefore pathological) side paradoxically inducedipsilesional extinction (Vuilleumier, 2000). These results suggestthat faces might exert some capture on spatial attention in neglectpatients despite their abnormal orienting bias towards the ipsile-sional side. Note that these effects could not simply be explained bya non-specific effect related to the right-hemispheric dominancefor facial processing (Grüsser & Landis, 1991), along the lines ofKinsbourne’s model (Kinsbourne, 1977). The latter model wouldpredict that this hemispheric dominance might lead to a reduc-tion of contralesional extinction whenever faces are presented tothe left or to the right hemifield, because a preferential activationof the right hemisphere by faces should improve attention orient-ing towards the opposite left side. This result, however, was notobserved in that study (Vuilleumier, 2000). In addition, this modelwould also predict the highest levels of contralesional extinctionwhen words are presented to the right hemifield in bilateral trials(e.g. a contralesional shape with an ipsilesional word should elicit

higher left extinction than a contralesional shape with an ipsile-sional face, due to increased activation of the left hemisphere inthis case). Again, this was not observed (Vuilleumier, 2000). Theresults rather indicate that the spatial distribution of extinction in

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eglect can be modulated by the relative relevance of the contrale-ional stimuli. Therefore, certain biologically and socially relevanttimuli, such as faces, might be slightly stronger in attracting atten-ion in conditions of sensory competition, and thus more resistantalthough not totally immune) to extinction or neglect when pre-ented on the “weak” side. A similar facilitation of face detectionn neglect has later been confirmed in other studies using bothchematic stimuli (Vuilleumier, 2002; Vuilleumier & Schwartz,001b) and realistic photographs (Fox, 2002b).

The mechanisms subserving these effects have yet to be fullyefined, but it is known that face recognition relies on highlypecialized processes (Bruce & Young, 1986; Grüsser & Landis,991) with specific neural substrates in extrastriate visual cor-ices (e.g. Eimer, 2000; George et al., 1999; Itier & Taylor, 2004;anwisher, McDermott, & Chun, 1997). Face processing involves

nitial structural encoding stages in the inferior occipital gyrusso-called occipital face area, OFA) and ventral fusiform gyrus (so-alled fusiform face area, FFA), which are typically preserved inost neglect patients (Vuilleumier, 2000), and might therefore

eceive sufficient inputs from earlier ventral visual pathways toccomplish face detection or recognition in a bottom-up manner,egardless of top-down spatial attention (Vuilleumier, 2000). Elec-roencephalography (EEG) recordings also suggest that early faceategorization stages may occur between 100 and 200 ms post-ace onset, as typically indexed by the occipito-temporal P100nd N170 ERP-components, respectively (Dering, Martin, Moro,egna, & Thierry, 2011; Eimer, 2000; Itier & Taylor, 2004) or the100 and M170 in magnetoencephalography (MEG; see Liu, Harris,

Kanwisher, 2002). These components were found to be stillormally (or partly) evoked to faces in the contralesional field,ven when extinguished (Di Russo et al., 2008; Vuilleumier, Sagiv,t al., 2001). It remains unclear, however, whether the N170 is gen-rated in the fusiform gyri and/or other cortical regions (George

t al., 1999; Kanwisher et al., 1997). In any case, both the behav-oral (Fox, 2002a; Vuilleumier, 2000) and neurophysiological dataVuilleumier, Sagiv, et al., 2001) converge to support the idea thatace analysis and categorization may take place in the intact early

ig. 1. Effects of emotion on visual extinction. (A) Rate of contralesional misses for 2 patienimultaneously, showing substantial reduction in extinction when pictures depicted spieatures in spiders and flowers consisted of almost identical partial segments. (B) Rate ofn either the contralesional or ipsilesional hemifield, when paired with a neutral ring shapompared to the neutral faces, in three patients (� and � Patient 1; � Patient 2; © Patien

A) Adapted from Vuilleumier and Schwartz (2001a). (B) Adapted from Vuilleumier and S

chologia 50 (2012) 1054– 1071

visual processing stages of the ventral occipito-temporal stream,before information from the contralesional field is influenced bytop-down attention and selected (or not) for conscious awareness(Driver, 1995; Rafal, 1994; Ward & Goodrich, 1996).

Over and above faces in themselves, faces with emotionalexpressions may exert further influences on spatial neglect. Anearly behavioral study in parietal patients (Vuilleumier & Schwartz,2001b) showed for the first time that faces displaying either angryor happy expressions, when presented on the contralesional hemi-field in bilateral displays, could substantially decrease extinctionrates as compared with neutral faces presented in otherwise simi-lar displays (Fig. 1B). The influence of emotional cues on extinctionoccurred even though face expression was not relevant to thetask, suggesting that such effects arose relatively independently ofovert attention (Vuilleumier & Schwartz, 2001b). Similarly, anotherstudy (Fox, 2002b) showed that spatial neglect was substantiallyimproved when contralesional stimuli were photographs of realfearful and happy faces, relative to images of fruits, but also rel-ative to neutral faces (Fox, 2002b). All these findings support thenotion that emotional expressions in faces may be even more effec-tive than neutral faces in alleviating the spatial biases of attentionassociated with parietal damage (Vuilleumier & Schwartz, 2001b).

The effect of facial emotions is not restricted to single/unilateralstimuli or extinction on double stimulation, but can also influencespatial neglect in visual search tasks with several simultaneouscompeting items. A recent study (Lucas & Vuilleumier, 2008) usedarrays with 8 faces including 7 identical individuals with a neu-tral expression plus one singleton, with a different identity, thatcould be cued by either a different shade of color (hence differingin both identity and color), or by a different emotional expression(hence differing in both identity and expression), or could be neu-tral and, hence, differing only in identity (Fig. 2A). Results showedthat both neglect patients and controls were, not only faster and

more accurate at detecting the color singletons (i.e. a typical fea-ture pop-out effect), but also at detecting the emotion singletons(both happy and fearful faces), as compared with face targets thatdiffered only in terms of their identity. Importantly, this cueing

ts with neglect and extinction (SV and EN) when two visual stimuli were displayedders, as compared to neutral pictures such as flowers or rings. Note that physical

extinction for faces displaying either angry or happy expressions, when presentede on the other side. Emotional faces showed significantly lower extinction rate, as

t 3) who had left neglect and extinction.

chwartz (2001b).

J. Domínguez-Borràs et al. / Neuropsychologia 50 (2012) 1054– 1071 1059

Fig. 2. Effects of emotion on visual search. (A) Illustration of two different conditions with either a neutral (upper) or fearful (lower) target in a task where neglect patientshad to search and report the gender of the face with odd-out identity. (B) Average response times in 13 neglect patients showed better detection of face singletons, among 7other neutral faces when those singletons depicted a fearful expression (therefore differing in both identity and expression; ID + FEAR), as compared to a neutral expression(that is, differing only in identity; ID only). This emotional cueing benefit was found for stimuli presented in both visual hemifields, in combination with generally slowerresponse times to contralesional targets. Healthy controls showed similar emotional cueing effects, but no spatial asymmetry or even a left-side advantage (data not shown)(C) Lesion-symptom mapping in the same patients showing areas correlating with the magnitude of the difference in RTs for neutral minus emotional faces. Damage to thep cues

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osterior temporo-parietal junction was associated with larger effects of emotionalmaller effects of emotional cues (blue). (For interpretation of the references to colo

dapted from Lucas and Vuilleumier (2008).

ffect (by color or by expression) was observed equally for stimuliresented in the left (neglected) and right (intact) visual hemifieldsFig. 2B), in both groups of participants, despite the fact that neglectatients were generally slower in detecting singletons in the con-ralesional than in the ipsilesional side. Thus, the attentional biasowards salient emotional stimuli, just like color pop-out, appearedo operate independently from (and additively to) the patholog-cal bias towards the ipsilesional side of space, suggesting twoistinct sources of influences on visual attention. In other words,

eft spatial neglect still impaired detection of left-sided targets,elative to the right-sided targets, but the former benefited fromhe same emotional advantage as the latter. Therefore, this studyemonstrated not only that spatial cueing effects by emotionalace expression occurred even for a difficult task with numerousistracters, rather than just for extinction tasks, but that theseffects were mediated by visual mechanisms presumably sparedy the lesion and distinct from those controlling voluntary atten-ion. Moreover, the results were unlikely to be simply explainedy low-level perceptual differences because all faces had similar

uminance, size, eye or mouth position, and were controlled fornterstimulus perceptual variance (ISPV) across conditions (Lucas

Vuilleumier, 2008). These findings also converge with studies onisual search in normal observers showing that emotional faces

end to be detected faster than neutral faces, even in the presencef increasing distractor load (Eastwood, Smilek, & Merikle, 2001;hman, Lundqvist, & Esteves, 2001; Williams, Moss, Bradshaw, &attingley, 2005).

(red-orange), whereas anterior lesions in orbitofrontal regions was associated withhis figure legend, the reader is referred to the web version of the article.)

Besides faces and facial expressions, it has also been found thatpatients with neglect and extinction show a better detection rate ofstimuli presented contralesionally in bilateral displays when theydepicted spiders, known to elicit strong emotion-related physio-logical responses in humans (e.g. see Blue, 2010), as compared towhen contralesional stimuli were neutral pictures, such as flow-ers (Vuilleumier & Schwartz, 2001a; Fig. 1A). Again, these findingscould not be explained by differences in physical features, suchas contrast, spatial frequency or brightness, as both spiders andflowers consisted of almost identical local elements (see Fig. 1A).Spiders are also known to be detected better and faster than neu-tral objects in visual search tasks in healthy people (Ohman, Flykt,& Esteves, 2001). Again, these data corroborate that emotionalstimuli might still have the same advantage in capturing atten-tion despite damage in parietal cortical areas involved in spatialattention (Vuilleumier & Schwartz, 2001a).

Another recent study by Tamietto and colleagues (Tamietto,Geminiani, Genero, & de Gelder, 2007) demonstrated that sim-ilar emotional effects could be observed for bodily expressionsand gestures. Patients presenting neglect extinguished less oftencontralesional images of fearful bodily expressions than contrale-sional neutral or happy body gestures; and similarly as for faces(Vuilleumier, 2000), they extinguished more often the contrale-

sional neutral stimuli when the concurrent ipsilesional imagedepicted fearful body expressions. As the visual processing ofhuman body shape and bodily expression relies on dedicated brainregions in occipito-temporal cortex (so-called extrastriate body

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rea, EBA, and fusiform body area, FBA; see Peelen & Downing,005), these effects might again result from residual bottom-upnalysis at early perceptual stages since these visual pathways areresumably intact in many neglect patients. Furthermore, it is pos-ible that fronto-limbic areas might also activate in response tomotional threat gestures and thus promote reorienting of atten-ion and preparation to act (Tamietto et al., 2007). These authorsherefore postulated that such effect of gestures may reflect aorrespondence between perceiving and acting, which could beinked to the so-called “motor contagion” or “motor resonance”henomenon (Gallese, Keysers, & Rizzolatti, 2004; Levenson, 2003;amietto et al., 2007). An action-based account was similarly pro-osed to explain why extinction can be reduced when viewingbjects with instrumental properties (e.g. the handle of a cup ini Pellegrino, Rafal, & Tipper, 2005).

Finally, emotional scenes with multiple elements were alsoeported to partly overcome contralesional inattention in neglectatients. In this study, pictures from the IAPS (International Affec-ive Picture System) database (Grabowska et al., 2011) wereresented unilaterally to the left or right side of fixation in patientsith intact visual fields but stable USN. While neutral scenes were

ften not detected, emotional scenes were significantly more ofteneported. The nature of emotional cues varied across stimuli butas not systematically compared. Since many pictures included

aces, people, or animals, these effects are likely to result from sim-

lar emotional mechanisms as those observed in previous studiesFox, 2002b; Vuilleumier & Schwartz, 2001a, 2001b), but furtheremonstrate that they may still arise in conditions with multipletimuli within the same hemifield.

ig. 3. Effects of emotion on auditory extinction. (A) Pairs of voices uttering meaningledichotic listening), and could contain neutral prosody or both sides or emotional prosody

reduction of contralesional auditory extinction for all emotional relative to neutral voicere matched for duration and energy. (B) Lesion-symptom mapping in the same patient

or neutral minus emotional faces Benefits of emotional prosody were reduced by lesions

dapted from Grandjean et al. (2008).

chologia 50 (2012) 1054– 1071

Interestingly, residual processing of contralesional stimuli maytake place not only in vision but also in other sensory modalitiessuch as tactile perception (Berti et al., 1999) and audition (Deouell,2002). However, only few studies have investigated the effect ofaffective cues on neglect or extinction in non-visual modalities.For instance, in a recent study of six neglect patients (Grandjean,Sander, Lucas, Scherer, & Vuilleumier, 2008), pairs of vocal stimuliwere presented to both ears simultaneously (dichotic listening) andcould contain emotional prosody on one side (fear, anger, or hap-piness) plus neutral on the other side, or neutral prosody on bothsides. Emotional voices presented to the left ear reduced contrale-sional auditory extinction more than neutral voices (Fig. 3A). Again,this effect was not explained by low-level acoustic differences sincevoices were all matched for duration and energy (Grandjean et al.,2008). These findings indicate that emotional facilitation of spa-tial attention and awareness in neglect patients might reflect ageneral advantage of emotional saliency in perception, expressedin a multisensory manner rather than limited to a single sensorymodality.

All together, these findings in patients with neglect and/orextinction add to previous neuropsychological evidence that thedistribution of attention in space can be modulated by perceptualfactors reflecting residual detection and organization of sensoryinformation from the contralesional side, based on particular stim-ulus characteristics, and despite preferential attention biases to

the other side. More specifically, these data demonstrate thatemotional significance may also benefit from such residual pro-cessing, and that additionally it has a direct functional impact onattention which can partly overcome (or counteract) neglect or

ss syllables were presented simultaneously with one stimulus heard in each ear on either the left or right side. Average detection rates in 6 neglect patients showedes. This effect could not be explained by low-level acoustic differences since voicess showing areas correlating with the magnitude of the difference in extinction rate

extending in right posterior OFC.

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xtinction. These findings also converge with research in healthyndividuals (e.g. Carretie, Hinojosa, Martin-Loeches, Mercado, &apia, 2004; Hansen & Hansen, 1988; Ohman, Lundqvist, et al.,001; Richards & Blanchette, 2004; Vuilleumier, 2005a) andome psychiatry conditions (e.g. anxiety; Flykt & Caldara, 2006;ox, 2002a) showing that emotional stimuli tend to be priori-ized within the sensory systems such that they elicit faster andtronger attention capture, obtaining privileged access to aware-ess in conditions of perceptual competition between multipletimuli.

Note however that residual emotion processing may alsoe observed in the contralesional hemifield without any direct

mpact on subsequent orienting of spatial attention. For instance,illiams and Mattingley (2004) showed that faces with emo-

ional expression appearing in the left visual field could influenceask performance even when they are not seen consciously. Theseuthors asked a patient with extinction to make a speeded emo-ion judgment (sad vs. happy) for a single face target presentedt the screen center, which was preceded by two prime facesriefly flashed in the left and right visual field, one upright (withither a sad or happy expression) and one inverted (with a neu-ral expression). Response times to the central face target wereignificantly slowed when the upright peripheral face displayedn incongruent expression as compared with this central face,egardless of whether it appeared in the left or right visual field.mportantly, the patient was at chance in detecting the presencef the left-side face. Therefore, these data confirm that emotionxpression can be implicitly extracted from contralesional fieldespite neglect. It remains to be seen whether other emotionaltimuli and which emotional categories or dimensions (valence,rousal) account for these effects. It also remains to be determinedhether other implicit effects broadly attributed to unconscious

ision might (at least partly) be mediated by emotional processess well. For instance, a classic phenomenon of unconscious percep-ion was reported by Marshall and Halligan (1988) in a patient whoas presented simultaneously with two drawings of a house, one ofhich depicted the left side of the house on fire. When the patientas asked to select which house she preferred, she consistently

hose the house that was not burning, even though she judged thathe two drawings were identical when asked to compare them.uch biases in preference could potentially be accounted by implicitffective appraisal, or alternatively by some unconscious detectionf visual anomalies in the contralesional visual information (seelso Bisiach & Rusconi, 1990).

More generally, the extent to which emotional facilitation onttention is comparable to the classic pop-out effect, and whethert is due to physical features or truly affective categorization, haseen repeatedly questioned in research investigating these effects

n normal people (e.g. see Coelho, Cloete, & Wallis, 2010; Foxt al., 2000; Huang, Baddeley, & Young, 2008; Huang & Yeh, 2011;uilleumier, 2005a; Vuilleumier & Huang, 2009; Vuilleumier &chwartz, 2001a). A first issue is that it is possible that some low-evel elements in emotional stimuli might be salient by themselvesnd drive attention without requiring an engagement of emotionalystems. This could arise either because of non-controlled con-ounding factors (e.g. Purcell & Stewart, 2010; Purcell, Stewart, &kov, 1996) or because of systematic featural or configural changesnduced by the distinctive expression cues (Coelho et al., 2010;hman, Lundqvist, et al., 2001; Schubo, Gendolla, Meinecke, &bele, 2006). However, it is also possible that even simple visual

eatures that are “diagnostic” for (or statistically correlated with)articular emotional stimuli may be sufficient to associate with

he corresponding emotional meaning, and thus activate affec-ive or motivational systems based on very low-level cues – suchs wide-open eyes in faces (Whalen et al., 2004) or sharp andpiky edges in objects (Bar & Neta, 2007; see also Vuilleumier,

chologia 50 (2012) 1054– 1071 1061

Armony, Driver, & Dolan, 2003). Moreover, a role for emotionalrather than just perceptual appraisal is supported by the findingsthat attentional effects are specific to fear-relevant categories inphobic patients (e.g. faster visual search for pictures of snakes thanspiders in snake phobics, but vice versa in spider phobics; see Flykt& Caldara, 2006; Ohman, Flykt, et al., 2001), and that some physi-ological bodily responses can be evoked by unattended emotionalstimuli, but not by their features in isolation (Flykt, 2005). A secondissue is that more rapid orienting of attention and more efficientdetection of emotional stimuli among distracters, as observed inthe so-called face-in-the-crowd effect in normal subjects (Hansen& Hansen, 1988) or visual search tasks with pictures of snakesand spiders in phobics (Ohman, Lundqvist, et al., 2001), may notnecessarily imply that search is not serial and emotion stimuli pro-cessed in parallel independent of the amount of distracters (Foxet al., 2000; Vuilleumier, 2005a). In fact, visual search studies haveshown linear increases in target detection latencies as a functionof distracter number for both emotional and neutral targets, butwith a shallower increase in slope for the former compared tothe latter (e.g. Eastwood et al., 2001; Smilek, Frischen, Reynolds,Gerritsen, & Eastwood, 2007). This indicates that emotional stimuliare more efficient in guiding attention towards their location andcan thus attenuate (but not abolish) the competition induced bythe presence of concurrent distractors (see also Smilek et al., 2007).Likewise, neuropsychological findings in neglect patients show thatfor emotional stimuli, just like for neutral stimuli, search times arestill abnormally prolonged (Lucas & Vuilleumier, 2008), and extinc-tion rates on double simultaneous stimulations are always higherin the contralesional than in the ipsilesional field (Fox, 2002b;Vuilleumier & Schwartz, 2001a, 2001b). This clearly indicates thatemotional stimuli do not by-pass serial and attention-demandingprocesses to be perceived and reported, but that their likelihoodof attracting attention tends to be greater, due to additional biaseswhich may operate in parallel (simultaneously with) the top-downmechanisms of attention. Accordingly, recent studies using brainimaging techniques, in both patients and healthy participants, havebegun to unveil specific neural networks that subserve emotionalbiases in perception and have distinct sources but similar effectson sensory pathways.

4. Neural substrates of attention and impaired awarenessin spatial neglect

Over the past decades, attention has been shown to play a cru-cial role for stimulus-awareness (Beck, Rees, Frith, & Lavie, 2001;Dehaene et al., 2006; Driver & Mattingley, 1998), and is now widelyrecognized to act on perception by enhancing the neural repre-sentation of target stimuli (Desimone & Duncan, 1995). Becauseprocessing resources are shared across different receptive fields(e.g. different locations on the retina in the visual modality) andare inherently limited (Kanwisher & Wojciulik, 2000), concurrentstimuli in the environment will compete for access to higher stagesof perceptual processing and guide behavioral responses (Rafal,Danziger, Grossi, Machado, & Ward, 2002). Endogenous attentioncan boost the neural representation of one stimulus over othersand thus act to increase its perceptual saliency through top-downsignals that modulate neural activity in sensory pathways. Evenwhen two stimuli overlap at fixation, directing attention to onestimulus will selectively increase activity in brain areas coding forthis stimulus, practically to the same degree as when the stimulusis presented alone; while the representation of the other stimu-

lus will be attenuated and its perception limited or even abolished(O’Craven, Downing, & Kanwisher, 1999; Vuilleumier, Sagiv, et al.,2001). Conversely, when a stimulus is intrinsically more salientdue to some unique feature (e.g. pop-out) or gestalt organization

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e.g. grouping), it will have a stronger weight in the competitionnd attract more attention through bottom-up processes (Beck &astner, 2009). Emotional processing may act in a similar man-er by boosting the neural response to (and hence the saliencyf) biologically or motivationally significant information relative toeutral stimuli (Vuilleumier, 2005a), but as we will describe below,hese effects may not easily be attributed to purely top-down orottom-up mechanisms. Rather, they seem to fall in-between thesewo traditional categories (Vuilleumier & Brosch, 2009).

Note also that the precise link between attention, stimulus-elated activation, and consciousness still remains under discus-ion, because no single brain area seems to subserve activity thats both necessary and sufficient to generate a conscious perceptRees, 2007), and because enhanced activity in sensory areas alones insufficient to produce awareness (e.g. intense occipito-temporalctivations can occur with a complete lack of conscious report,ee Dehaene et al., 2006). Thus, many current theories of aware-ess propose that, to give rise to conscious experience, a robusterceptual representation in sensory areas must be accompaniedith concomitant activity in higher-level areas in frontal and pari-

tal regions which serves to maintain this sensory activity ando broadcast the corresponding representation to other brain sys-ems (Beck et al., 2001; Dehaene et al., 2006; Lamme, 2003). Thisroposal converges with accounts of neglect and extinction thatttribute these losses in awareness to deficits in sensory modu-ation and coupling with fronto-parietal systems responsible forttention, subsequent to focal damage in critical brain areas (Driver

Vuilleumier, 2001a).In support for this account, studies using fMRI in parietal

atients with spatial neglect and extinction have revealed con-istent functional anomalies in structural intact brain regionsorrelating with changes in perceptual performance. For exam-le, when presenting bilateral stimuli to both visual hemifieldsimultaneously, the contralesional (left-sided) objects may bextinguished from awareness, but nonetheless still activate thearly striate and extrastriate visual areas in the damaged (right)emisphere (Rees et al., 2000; Vuilleumier, Schwartz, Clarke,usain, & Driver, 2002; Vuilleumier, Sagiv, et al., 2001). No suchctivation is seen when presenting a single unilateral stimulusn the ipsilesional (right-sided) hemifield, although the consciouseport by the patient is identical in both cases (patients will alwayseport seeing a single stimulus on the right side). Moreover, whenhe extinguished stimuli are faces, only a weak residual activa-ion is seen in face-selective areas of the fusiform gyrus, whichould be consistent with an important role of activity in this region

or representing the specific content of stimulus awareness (Beckt al., 2001; Tong, Nakayama, Vaughan, & Kanwisher, 1998). Byontrast, conscious perception of contralesional faces, as opposedo extinction, will produce enhanced activations in several visualreas (striate cortex, cuneus, bilateral fusiform gyri) of the rightemisphere as well as intact parietal and prefrontal areas of the

eft hemisphere (Rees et al., 2002; Vuilleumier, Armony, et al.,002). Similar patterns were found for somatosensory processinguring tactile extinction in other patients (Sarri, Blankenburg, &river, 2006; Valenza, Seghier, Schwartz, Lazeyras, & Vuilleumier,004). Likewise, activation of intact areas in right occipital cortex inesponse to unilateral left visual stimuli can be reduced when thettentional load of a task at fixation is increased (Vuilleumier et al.,008), a manipulation that typically exacerbates spatial neglect inatients in various behavioral tasks. This reduction in the damagedemisphere during attention to a central task tends to be modest

n the early visual cortex (e.g. V1 and V2) but more severe in higher

tages such as V4, where increased attention to the central taskay totally abolish the neural response that would otherwise be

voked by the same stimulus without concurrent competition forttention.

chologia 50 (2012) 1054– 1071

Therefore, as observed for stimuli presented in unattended con-ditions in normal observers (O’Craven et al., 1999; Vuilleumier,Armony, et al., 2001), residual activation can still be elicited byunperceived or neglected stimuli in the contralesional side inparietal-damaged patients, but it is weaker, limited to sensoryareas (in comparison with perceived stimuli) and tends to be fur-ther attenuated when attention is engaged by other task-relevantstimuli. These findings do not only provide a neural substrate forimplicit or unconscious processing in neglect (Driver & Vuilleumier,2001b) but also indicate that weak, purely bottom-up, activationsof sensory pathways may not be sufficient to produce consciousperception when severed from interactions with top-down signalsfrom parietal-frontal areas. Similar conclusions have generally beenreached by studies using ERP measures in patients, although somedivergences still remain between different paradigms and differentERP components (Vuilleumier, 2005b). In particular, extinguishedfaces were found to elicit residual face-specific N1 and N170 poten-tials (Vuilleumier, Sagiv, et al., 2001; see also Di Russo et al., 2008– for simpler stimuli) whereas P1 was found to be either intact (DiRusso et al., 2008; Vuilleumier et al., 2008) or reduced (Driver et al.,2001; Marzi et al., 2000) in different patients, and later visual ERPs(such as N1p, P2, or P3) were always markedly affected. Similar pat-terns of effects were also observed for somatosensory ERPs duringtactile extinction (Eimer, Maravita, Van Velzen, Husain, & Driver,2002). Thus, again, these data suggest that some residual (perhapsweakened) activity may take place in early sensory areas whilesubsequent processing stages might be disrupted due to the lossof top-down feedback signals from the damaged parietal/frontalareas. This lack of sensory enhancement by fronto-parietal sys-tems might prevent information from the contralesional space tocompete effectively for attention.

An emerging view on the influence of emotion on perceptionis that a reduction in cortical sensory responses (due to fronto-parietal damage in patients or to inattention in normal subjects)might be counteracted by a distinct source of enhancement medi-ated by emotion processing systems. But how do emotional signalsoperate to boost stimulus processing and attention, and how canthey actually help improve neglect symptoms? Although thereis still much ongoing debate concerning these issues, a key roleis likely played by neural circuits that remain intact in neglectpatients, assuming that their functioning is not a consequence ofpost-lesion plasticity (Tamietto & de Gelder, 2010). It is even pos-sible that lesions in parietal and lateral prefrontal areas may notonly leave emotional influences relatively intact, but even tend toenhance them due to the reduced control by top-down attention(Vuilleumier, Armony, et al., 2002; Yamasaki, LaBar, & McCarthy,2002). In particular, the amygdala, a complex nucleus located inthe anterior medial temporal lobe and involved in a wide rangeof emotional processes, is generally suspected to play a crucialrole by projecting to sensory areas and enhancing their responseto emotionally significant information (Freese & Amaral, 2005;Vuilleumier, 2005a). Such enhancement might in turn be respon-sible for the greater saliency of these stimuli and their strongercompetition weight for the capture of attention.

5. Neural substrates for emotional influences on attentionand spatial neglect

Initial evidence in support of the idea that the amygdala maycontribute to enhance brain responses to stimuli in neglected spacewas provided by one fMRI study comparing visual extinction for

neutral or fearful faces in a patient with focal parietal damage(Vuilleumier, Armony, et al., 2002). This patient had intact visualfield, but stable neglect and visual extinction on bilateral simul-taneous stimulation. During fMRI, on each trial (in unpredictable

J. Domínguez-Borràs et al. / Neuropsychologia 50 (2012) 1054– 1071 1063

Fig. 4. Functional MRI results during visual extinction for faces. (A) Illustration of the task performed by the patient, in which a face could appear in the LVF either alone(unilateral trials) or paired with a house in the other visual field (bilateral trials), with either a neutral or fearful expression, and be either consciously perceived or extinguished.(B) Activity was evoked in the right fusiform cortex (upper panel) by consciously seen faces, as opposed to seen houses, irrespective of emotional expression and field ofpresentation; whereas the left amygdala, left lateral orbitofrontal cortex, and bilateral fusiform cortex (lower panel) was activated by faces with a fearful expression, as opposedto neutral expression, w, irrespective of field of presentation. Moreover, activity in the fusiform cortex, but not left amygdala and orbitofrontal cortex, was modulated byawareness of the faces, as opposed to extinction. (C) Activity (beta values, arbitrary units) is plotted for the same three regions. The right fusiform cortex showed increaseswhen faces were consciously perceived, as opposed to extinguished, irrespective of emotional expression, but also enhanced responses to fearful as compared to neutralexpression, both when the faces were perceived and extinguished. The left amygdala showed increases to fearful faces both when consciously perceived and extinguished,b en thet

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ut also a weak response to neutral faces when these were extinguished (unlike whhan neutral faces, during both conscious perception and extinction.

dapted from Vuilleumier, Armony, et al. (2002).

rder), a picture of a face was briefly presented in the left visual fieldLVF) or right visual field (RVF), either alone or accompanied by aimultaneous picture of a house on the opposite side. Faces couldave either a neutral or fearful expression (Fig. 4A). On bilateralrials, the patient missed slightly but significantly fewer left-sidedearful faces (63%) than left-side neutral faces (68%), but interest-ngly this difference was more pronounced in the first part of theesting (55% vs. 75%) and then habituated. There was no differ-nce for unilateral left-sided faces presented alone (37% missed inoth cases). The fMRI results showed that the occipital cortex wasctivated by all faces presented in the LVF, irrespective of whetherhey were perceived or neglected, whereas the right fusiform face-esponsive area (FFA) in temporo-occipital cortex was activated byeutral faces only when these were perceived, whereas it did notespond differentially (as compared with houses) when faces extin-

uished (Fig. 4B and C). By contrast, fearful faces in the LVF producednhanced responses in the right FFA (compared to neutral faces) notnly when perceived, but also when extinguished, such that thisegion now responded differentially to the unseen face stimulus

se were consciously seen). The orbitofrontal cortex also responded to fearful more

(as compared with a house; Fig. 4B and C). Such increase in visualresponses to fearful faces might therefore account for their relativeresistance to extinction by a competing stimulus (house) on theipsilesional side and the corresponding enhancement of perceptualawareness. Note, however, that fusiform activation to the extin-guished fearful faces was still lower than that to perceived faces,in keeping with reduced awareness on those trials. Importantly,fearful compared to neutral faces also evoked increased neuralresponses in left amygdala, left orbitofrontal cortex (OFC), and rightsuperior parietal cortex (all spared areas outside the lesion), acrossall bilateral trials, irrespective of whether the left-side face was per-ceived or extinguished. This would be consistent with those regionsbeing differentially recruited by emotion signals prior to attentionand in turn triggering top-down modulation of fusiform responsesthat would not occur otherwise for neutral stimuli.

Another recent fMRI study (Grabowska et al., 2011) used com-plex pictures (scenes from the IAPS) presented unilaterally (inRVF or LVF, always alone). These scenes depicted people, animals,and various other situations. Results confirmed that emotional

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nformation can partly overcome contralesional neglect and stillroduce differential neural responses despite impaired atten-ion. Compared to neutral scenes, emotional scenes presented inhe LVF were more frequently reported (48% vs. 43%) and pro-uced increased activity in anterior extrastriate regions includingarahippocampal cortex (possibly overlapping with areas respond-

ng to places – Downing, Chan, Peelen, Dodds, & Kanwisher, 2006 or complex meaningful objects – Vuilleumier, Henson, Driver, &olan, 2002). However, no increase was found in the amygdala in

his study for emotional scenes relative to neutral scenes even whenhese were perceived and/or presented in the RVF. As the amygdalas usually highly responsive to such material (e.g. Sabatinelli et al.,011; Vrticka, Sander, & Vuilleumier, 2011), this negative resultight reflect a lack of power or signal drop-out. On the other hand,

his study found that emotional scenes compared to neutral sceneslso activated the anterior cingulate cortex (ACC), when presentedn either visual field, which was interpreted as potentially reflect-ng emotional arousal and as providing a source of subsequentop-down modulation.

Such increase in visual responses to emotional faces (or otherisual stimuli) is consistent with a wide body of neuroimagingnvestigations (using PET, fMRI ERPs, or MEG), in healthy individu-ls, that have shown enhanced processing of affective information,elative to neutral stimuli. These effects have been observed inace-selective regions such as fusiform cortex with emotional facese.g. de Gelder, Morris, & Dolan, 2005; Vuilleumier, Armony, et al.,001), body-responsive areas in occipital cortex for expressive ges-ures (Peelen, Atkinson, Andersson, & Vuilleumier, 2007), otherarly visual areas with non-human visual stimuli (e.g. Bermpohlt al., 2006; Sabatinelli, Lang, Bradley, Costa, & Keil, 2009), and inarly auditory regions with emotional vocalizations and prosodyEthofer et al., 2011; Fecteau, Belin, Joanette, & Armony, 2007;randjean et al., 2005). ERP findings also suggest that such emo-

ional biases may occur early in the cortex, between 90–100 msnd 130 ms after stimulus onset for the visual modality (Pourtois,randjean, Sander, & Vuilleumier, 2004; Rotshtein et al., 2010;tolarova, Keil, & Moratti, 2006), often prior to a full visual cate-orization stage (Vuilleumier & Pourtois, 2007). This enhancementf sensory responses to emotional stimuli compared to neutraltimuli is in many ways comparable to the enhancement observedor attended vs. non-attended objects (see Kastner & Ungerleider,001; Vuilleumier & Driver, 2007), or attended vs. ignored stimu-

us features (Hillyard & Anllo-Vento, 1998; Luck & Hillyard, 1994;hang & Luck, 2009).

Furthermore, a causal role of the amygdala in such top-downodulation is suggested by anatomical studies in the monkeyhich demonstrated that this structure does not only receive

ich sensory inputs (from all modalities) but also sends projec-ions back to many sensory areas (see Amaral et al., 2003). At the

icroscopic level, these projections from amygdala to visual areaserminate exclusively in superficial layers of the cortex (Freese &maral, 2005), and display a characteristic pattern that is consis-

ent with excitatory feedback inputs to pyramidal neurons in thesereas (Freese & Amaral, 2006). Furthermore, projections to visualreas have a precise topographical organization, with a rostral-to-audal gradient such that more rostral regions of the amygdalaroject to higher-level areas in rostral parts of the ventral temporaltream (e.g. area TE), whereas more caudal regions of the amyg-ala project to more caudal visual areas (e.g. V1), suggesting thatoth early and later stages of visual perception can be influencedy the amygdala. In addition, amygdala nuclei (basal and baso-

ateral) also project to (Freese & Amaral, 2005) auditory (LeDoux,

000) and somatosensory cortices (Friedman, Murray, O’Neill, &ishkin, 1986). Therefore, the amygdala is ideally positioned to

xert a direct modulatory control over sensory processing in differ-nt modalities, and this modulation involves neural pathways that

chologia 50 (2012) 1054– 1071

are spared after typical parietal or frontal lesions associated withneglect. Indirect effects are also possible via projections from amyg-dala to cholinergic nuclei in the basal forebrain which then projectto widespread cortical regions and mediate more global arousalfunctions (Dringenberg, Saber, & Cahill, 2001; Sarter, Hasselmo,Bruno, & Givens, 2005).

This causal role of the amygdala is supported by the fact thatdamage to this structure may reduce the normal detection advan-tage for emotional stimuli in attentional blink tasks (Anderson &Phelps, 2001; but see Bach, Talmi, Hurlemann, Patin, & Dolan, 2011)and also abolish the increased response of visual areas to emotionalstimuli. Patients with epilepsy and mesial temporal lobe sclerosisshow normal activation to neutral faces in fusiform cortex and otherbrain regions, but no differential enhancement by the face expres-sion (Benuzzi et al., 2004; Vuilleumier, Richardson, Armony, Driver,& Dolan, 2004). Importantly, this loss of emotional effect in visualcortex is specific to patients in whom sclerosis affects the amyg-dala, but is not seen in those in whom sclerosis is limited to thehippocampus (Vuilleumier et al., 2004). This effect correlates withthe duration of epilepsy disease (Benuzzi et al., 2004). Remark-ably, the fusiform cortex is still modulated by attention in thesepatients (Vuilleumier et al., 2004), demonstrating that top-downmodulation by attention is preserved and has distinct sources. Thiscontrasts with the consequence of spatial neglect after parietallesion where activity in visual cortex is reduced due to impairedattention but preserved in response to emotion cues (Vuilleumier,Armony, et al., 2002). Likewise, an ERP study in epilepsy patientswith amygdala damage due to mesial temporal lobe sclerosis alsofound that the differential responses normally evoked by emo-tional faces were abolished at specific time-windows, namely inthe ranges of 100–150 ms (P1 component) and 500–600 ms (P3)post-stimulus onset, which may correspond to perceptual pro-cessing, as well as attentional orienting or memory, respectively(Rotshtein et al., 2010). By contrast, there was no effect of amygdaladamage on emotion-related ERPs at intermediate time-windows(150–250 ms), presumably related to explicit visual categoriza-tion processes. These findings suggest that amygdala damage maydirectly affect both perceptual-attentional and mnemonic process-ing, but not necessarily explicit emotion recognition (Rotshteinet al., 2010). Finally, in a different fMRI study, it was found thata pro-cholinergic drug (physostigmine) did not modify the dif-ferential modulation of visual cortex to fearful and neutral faces(Bentley, Vuilleumier, Thiel, Driver, & Dolan, 2003), indicating thatthese effects likely depend on direct (feedback projections) ratherthan indirect (via basal forebrain) influences from the amygdala.

Other indirect output routes from amygdala to perceptual andattentional systems might involve projections to OFC, which inturn has substantial direct connections with posterior parietal areasassociated with attention and eye movements (Cavada, Company,Tejedor, Cruz-Rizzolo, & Reinoso-Suarez, 2000). These pathwaysare thought to mediate motivational influences on parietal activ-ity observed in visuomotor tasks, although usually associatedwith reward/approach rather than aversive/avoidance behaviors(Bouret & Richmond, 2010; Maunsell, 2004; Platt & Glimcher,1999). A contribution of OFC to these effects is consistent withrapid single unit responses observed in this region (Kawasaki et al.,2005), as well as preserved fMRI activation to fearful faces inneglected field (Vuilleumier, Armony, et al., 2002) and anatom-ical lesion mapping studies on emotion–attention interaction inpatients (Grandjean et al., 2008; Lucas & Vuilleumier, 2008). In astudy investigating visual search for emotional and neutral facesin neglect (Lucas & Vuilleumier, 2008), it was observed that those

patients who benefited the least from cueing by emotion expres-sion had a lesion in OFC. Conversely, patients who benefited themost had lesions centered on frontoparietal areas, despite havingthe most severe neglect symptoms within the sample. This finding

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trongly suggests that the facilitatory effect of emotional processingn visual search was not due to sparing of fronto-parietal sys-ems normally mediating attentional processes, but rather throughistinct modulatory influences involving limbic prefrontal areasLucas & Vuilleumier, 2008). In a similar vein, in a study of auditoryxtinction for emotional and neutral voices (Grandjean et al., 2008),he severity of extinction symptoms was greater in patients witharietal damage, whereas the improvement of extinction symp-oms by emotional (vs. neutral) prosody decreased in patientsith lesions in right posterior OFC or lesions in superior tempo-

al regions associated with voice processing (see Grandjean et al.,005). Accordingly, damage to OFC may also impair explicit recog-ition of vocal emotions (Hornak et al., 2003).

Another recent study using binocular rivalry in healthy indi-iduals also supported the idea that detection of emotional facesas not determined by the activity of frontoparietal attentionaletworks, as was observed with neutral faces, but by an increased

unctional connectivity between the amygdala and areas in the ven-ral visual system directly (Amting, Greening, & Mitchell, 2010).

oreover, the authors found that inverse interactions between themygdala and the perigenual prefrontal cortex (pgPFC, Brodmann’sreas 32/10, implicated in regulating amygdala activity) might beritical to determine whether an emotional stimulus will over-ome binocular rivalry and be consciously processed, or contrarily,emain suppressed (Amting et al., 2010). The authors suggestedhat the degree of amygdala responses to suppressed stimuli wouldikely influence the threshold for consciousness, and thus act as aottom-up amplifier similar to attention, by interacting with phy-

ogenetically newer systems such as the ones described here (seelso Tamietto & de Gelder, 2010; Vuilleumier, 2005a, 2009). Thisccount is similar to the mechanisms presumably responsible forhe effects of emotional cues on spatial attention and perception ineglect patients (Kawasaki et al., 2001; Vuilleumier, Armony, et al.,002).

Because all these data support an important causal role of themygdala in boosting detection of emotional stimuli, and becausehe amygdala is critically implicated in classical aversive condi-ioning, in both animals and humans, it could be predicted that annhancement of perceptual processing may also occur for stimulihat acquired emotional significance through associative condi-ioning. We have directly tested this prediction in a patient withpatial neglect and chronic visual extinction by comparing per-ormance before and after pavlovian conditioning (unpublishedesults). The patient had to report red, blue, or green trianglesresented unilaterally or bilaterally on a screen, but the red tri-ngles were paired to an unpleasant burst of white noise during

brief conditioning session, taking place between two blocksf trials on the visual task. Before the conditioning session, theatient extinguished more than 40% of the left stimuli when pre-ented in bilateral trials. However, after conditioning, left-sideded triangles elicited not only fewer misses (less than 5%), butlso enhanced skin-conductance response. These changes suggest

striking enhancement of attention to stimuli in contralesionalpace when these stimuli have acquired a new affective (negative)alue. In addition, fMRI responses in the right fusiform cortex werencreased when processing emotionally significant stimuli (condi-ioned red triangles) in relation to neutral stimuli (unconditionedriangles). The amygdala was activated by the white-noise, as wells by the aversively conditioned red shapes after (not before) con-itioning, although these effects were weak. One possible reasonor weak amygdala activation in this study could be that the condi-ioning session was extremely short (with only a few parings of the

hite noise with red shapes). Moreover, the improved detection by

motional conditioning lasted for only a short time. Nevertheless,n parallel with the improvement in visual awareness, fMRI dataevealed that conditioning led to enhanced sensory responses in

chologia 50 (2012) 1054– 1071 1065

visual cortex when these stimuli were presented in the contrale-sional hemifield. These findings accord with an effect of emotionalbiases modulating attention towards relevant information, whichcan still act despite abnormal spatial attention in neglect patients.

In conclusion, further research is still needed regarding the neu-ral circuitry of these effects, as it seems plausible that emotionalprocessing might boost stimulus consciousness in neglect throughmore than one network. Although there is abundant evidencefor functional modulation from the amygdala on sensory areas(through direct feedback projections, or indirect projections viacholinergic or noradrenergic pathways, bypassing the frontopari-etal networks of spatial attention), other pathways via OFC, ACC, orpulvinar might also operate to enhance sensory processing via theirconnections to intact dorsolateral prefrontal and posterior parietalareas (Pourtois, Thut, Grave de Peralta, Michel, & Vuilleumier, 2005;Tamietto & de Gelder, 2010). This might explain why emotionalenhancement may occur sometimes in neglect patients even with-out (visible) amygdala activation (Grabowska et al., 2011) and/orwhy emotional enhancement may also persist in some patientswith temporal lobe (amygdala) lesions (Bach et al., 2011; Piechet al., 2011). Future studies should investigate these effects in largersamples of brain-damaged patients with various lesions, and/or useinterference methods such as TMS to better pinpoint their sourcesand time-course.

6. Preattentive pathways to the amygdala

The fact that emotional responses may occur for stimuli in theneglected field of parietal patients (e.g. Grabowska et al., 2011;Vuilleumier, Armony, et al., 2002) or outside attention in healthysubjects (e.g. Anderson, Christoff, Panitz, De Rosa, & Gabrieli, 2003;Vuilleumier, Armony, et al., 2001) in order to bias sensory com-petition and boost their access to awareness, begs the questionof how emotional inputs reach the amygdala prior to attentionselection (see also Pourtois, Spinelli, Seeck, & Vuilleumier, 2010).Although this issue still remains unresolved, several possible routeshave been suggested (Vuilleumier, 2005a) and may vary dependingon the paradigms or pathologies considered (Driver & Vuilleumier,2001b). One classic hypothesis originally suggested to account forblindsight after occipital lobe damage, is that some (rudimen-tary) visual signals would bypass visual cortex by projecting tothe superior colliculus and pulvinar before reaching the amygdala(de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999; Tamietto & deGelder, 2010). The amygdala might in turn modulate visual cor-tical areas in parallel to the incoming inputs received from thegeniculo-striate pathways, leading to enhanced sensory responses(in neglect) or influencing behavior without conscious percept (inblindsight). This pathway has been disputed (Pessoa & Adolphs,2010) because the superior colliculus is primarily connected withthe inferior pulvinar (Shipp, 2003), whereas the amygdala andlimbic areas are connected with medial pulvinar and connectionsbetween both regions of the pulvinar are not known in the macaque(Pessoa & Adolphs, 2010). Yet, anatomical studies in other pri-mates have revealed that visual responsive regions of the pulvinarthat receive input from superior colliculus have direct projectionsto both the amygdala and striatum (Day-Brown, Wei, Chomsung,Petry, & Bickford, 2010).

However, although this subcortical route may operate inpatients with blindsight, and perhaps become more efficient fol-lowing occipital lesion, other routes have also been suggested.For example, an alternative hypothesis is that visual inputs from

the pulvinar, bypassing V1 and other early cortical areas, projectdirectly to higher-level cortical regions (e.g. fusiform and ventraltemporal regions). In turn, the latter areas would project to theamygdala and the OFC (Vuilleumier, 2005a). Such projections from

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isual pulvinar to the fusiform and ventral temporal regions haveeen documented in humans (Clarke, Riahi-Arya, Tardif, Eskenasy,

Probst, 1999). Likewise, in parallel to the classic geniculo-striateathways, direct connections may also exist between the lat-ral geniculate nucleus (LGN) and higher-level extrastriate areasBullier & Kennedy, 1983; Schmid et al., 2010; Yukie & Iwai, 1981),hich may provide rapid visual inputs about motion and segmen-

ation cues in the visual scenes (Morand et al., 2000). Again, theseechanisms might contribute to emotional (and other) uncon-

cious effects in both neglect and blindsight patients (de Geldert al., 1999).

A third proposal that may account, not only for these effectsut also for similar findings in neurologically healthy individuals,

s a “dual stage” hypothesis, rather than a “dual route” hypothe-is (Vuilleumier, 2005a). In fact, it is well known from both humannd monkey neuroscience that visual processing might involve arst rapid feed-forward sweep of inputs projecting to widespreadreas in the brain (already shortly after 100 ms post-stimulusnset), including parietal and prefrontal cortices (Bullier, 2001;chmolesky et al., 1998), which is then followed by re-entranteedback signals that will influence the selection of behaviorallyelevant or meaningful information (Bar, 2003; Bar & Neta, 2007;amme, 2003). It is therefore conceivable that the amygdala (andther limbic regions such as OFC, see Kawasaki et al., 2001), justike posterior parietal and prefrontal cortices, may respond differ-ntially to some inputs at this early stage (i.e. when emotionallyignificant) and then by virtue of its projections to sensory areas,nfluence the subsequent perceptual processing and attention ori-nting.

Moreover, regardless of the exact anatomical pathway, it isikely that a rapid subcortical or a feedforward cortical route wouldarry only crude and partial information about stimuli. In particu-ar, it has been proposed that low spatial-frequency inputs (e.g. asonveyed by magnocellular visual pathways) might rapidly reacharietal and prefrontal areas directly from early visual corticesBullier, 2001; Pessoa & Adolphs, 2010; Vuilleumier, 2005a) andllow a rapid categorization of visual stimuli according to initialbest guesses” (Alorda, Serrano-Pedraza, Campos-Bueno, Sierra-azquez, & Montoya, 2007; Bar, 2003; Peyrin et al., 2010). Suchapid categorization for emotional meaning might also take placen the amygdala and/or OFC and operate on the basis of the initialhase of neuronal responses, prior to the accumulation of more reli-ble perceptual evidence in the cortex (Pourtois et al., 2010; Sugase,amane, Ueno, & Kawano, 1999). This hypothesis is also consis-ent with models of visual recognition where ultra-rapid visualncoding is thought to be enabled by cortical areas based on tim-ng characteristics of the very first spikes of neuronal responses,s opposed to the more traditional views on neural coding basedn firing rate (VanRullen & Thorpe, 2002). While potentially proneo errors, such a system would be useful for threat monitoringLeDoux, 2000; Ohman, Lundqvist, et al., 2001) and consistent withther findings on amygdala responsiveness to ambiguous informa-ion (Whalen, 2007).

Of course, a role for coarse, low spatial frequency informationn driving rapid visual responses in both the cortex and amygdalas specific to vision. Therefore, the nature of information responsi-le for rapid emotion processing in other modalities (e.g. audition)till remains to be determined. However, a coding scheme basedn the initial spiking response to some critical features of emo-ionally relevant stimuli (VanRullen & Thorpe, 2002) might affordimilar abilities across different senses. It is also worth noting thatlassic experiments on aversive conditioning in rodents have estab-

ished that simple auditory cues can elicit amygdala responses evenfter destruction of the auditory cortex; this is consistent with theiew that inputs bypassing early cortical processing stages maye sufficient in audition too. In any case, while such effects may

chologia 50 (2012) 1054– 1071

resemble emotion responses without consciousness in blindsightpatients (Anders et al., 2009; Morris, Ohman, & Dolan, 1999; Pegna,Khateb, Lazeyras, & Seghier, 2005), it remains to be seen whetherpre-attentive emotion effects in neglect depend on the same (e.g.subcortical) mechanisms, or instead on other (cortical) rapid sen-sory processes that can also operate in normal conditions (seeVuilleumier, 2005a).

7. Other modulations of spatial neglect by affective,motivational or social factors

All of the above effects of emotion cues on attention and per-ception (in both neglect and normal condition) have usually beenattributed to modulatory influences of the amygdala on sensorypathways (Anderson & Phelps, 2001; Vuilleumier, 2005a), andmost often related to the threatening or arousing dimensions ofemotional stimuli to which the amygdala is typically responding(LeDoux, 2000) but (see Sander, Grafman, & Zalla, 2003). However,other affective biases may exist and potentially also influence atten-tion, such as reward signals that are predominantly mediated byother neural systems centered on the ventral striatum and ventraltegmental area in the upper brainstem. Thus, electrophysiologicalstudies on parietal neurons implicated in attention and eye move-ments have consistently shown strong and early modulations ofactivity by expected reward value associated with target stimuli(Maunsell, 2004; Platt & Glimcher, 1999). It is likely that these influ-ences are driven by inputs from prefrontal areas such as OFC (Bouret& Richmond, 2010; Cavada et al., 2000), but reward signals havealso been observed in the superior colliculus (Ikeda & Hikosaka,2003; Weldon, DiNieri, Silver, Thomas, & Wright, 2007), whichmay also impact attentional orienting. In addition, experimentsin humans show that the reward value associated with targets invisual search tasks modulates correct detection rates and speed(Hickey, Chelazzi, & Theeuwes, 2010), or for instance, facilitates tac-tile discrimination judgments, as well as hemodynamic responsesin the corresponding primary somatosensory cortices (Pleger,Blankenburg, Ruff, Driver, & Dolan, 2008). However, the exact brainmechanisms underlying these effects are still poorly known.

In keeping with these findings, a recent study (Lucas et al.,2005) compared such reward effects in a group of neglect patientsand healthy controls who were asked to perform a visual search-guessing task. Subjects were presented with an array of itemsequally distributed over a screen, each of which could be associatedwith a different amount of points to gain or with no gain. Subjectswere instructed to “guess” and find the target with the highest gainin order to gain as many points as possible across successive trials.After selecting one item on a touch-screen, a feedback message waspresented to inform the subject about the gain associated with thejust chosen target, together with the cumulative amount of pointsgained up to that moment. Critically, the experiment manipulatedthe spatial distribution of the probability and amount of reward forchosen targets. In our subgroup of subjects, different gains wereobtained from the most left-sided to the most right-sided posi-tion of items. In a different subgroup, a symmetric distribution ofreward was presented. The results showed that in the first case,both healthy subjects and neglect patients progressively shiftedtheir choice towards the rewarded side, regardless of the visualhemifield (Lucas et al., 2005). No change in average choice distri-bution occurred in the second case. Importantly, this effect waspresent even when subjects were unaware of the reward distribu-tion biases when asked in an explicit debriefing questionnaire. Theneural substrates of these effects are unknown, but might impli-

cate connections from striatum and OFC to intact parietal areasand/or superior colliculi (Bouret & Richmond, 2010; Cavada et al.,2000; Ikeda & Hikosaka, 2003; Weldon et al., 2007) or even theamygdala since this region is also associated with reward learning

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Baxter & Murray, 2002). Beneficial effects of positive emotions onpatial attention in neglect patients have also been observed withleasant music (Soto et al., 2009), but these effects are presumablyediated by changes in affective state and arousal rather than by

irect impact of music on sensory or oculomotor systems.Spatial attention can also be influenced by other motivationally

ignificant cues without emotional meaning, such as eye gaze direc-ion in seen faces. Thus, in healthy people, seeing a face with eyes (oread) deviated to the right or left side will induce a reflexive shiftf attention towards the gazed-at location (Nummenmaa & Calder,009; Ristic, Wright, & Kingstone, 2007). Likewise, a behavioraltudy in neglect patients (Vuilleumier, 2002) also demonstratedhat the gaze direction of a face presented at the center of the screenould attenuate extinction of contralesional visual targets whent was directed to that side. This occurred even though the facend gaze information was task-irrelevant, and therefore patientsid not have to report or discriminate it. In another experimentVuilleumier, 2002), presenting an ipsilesional face looking towardshe contralesional side could also facilitate the detection of targetshat would otherwise be extinguished in most trials. In contrast,hen the ipsilesional face looked straight, contralesional extinc-

ion persisted. No effect on visual extinction was observed whenaces presented contralesionally looked towards the ipsilesionalemifield. This evidence suggested that gaze processing is not pre-ttentive, that is, that attention to the stimulus is needed to exertuch facilitatory effects (Vuilleumier, 2002). Nonetheless, gazeas task-irrelevant and thus affected spatial attention implicitly,espite a severe deficit in orienting attention to the contralesionaleld in other conditions. This suggests that this facilitation may alsoartly be independent of the spatial attention mechanisms that areediated by fronto-parietal areas and damaged in these patients,

ut the exact neural substrates have yet to be clarified. Visual cuesbout other people’s direction of gaze provide important informa-ion, indicating locations of potential interest in the environmentVuilleumier, 2002) and, like facial expression, is crucial for socialommunication (Frischen, Bayliss, & Tipper, 2007; Kleinke, 1986).euroimaging studies in healthy controls have also revealed thaterceived gaze direction activate parietal and temporal areas thatre both common and specific for gaze and other attention orient-ng mechanisms. Furthermore, a possible role of the amygdala waslso suggested by behavioral studies reporting that patients withemporal lobectomies (Akiyama et al., 2007; Okada et al., 2008)r amygdala lesions (Akiyama et al., 2007) did not show reflexivehifts to the direction of gaze in seen faces. Finally, an effect of eyeaze contact has also been shown to increase extinction (Maravitat al., 2007), whereby contralesional extinction is reduced whenested in the presence of a central face with closed eyes relativeo a central face with open eyes. This was interpreted as reflectingreater capture of attention resources in the latter case due to theocial significance of eye contact. Although the amygdala has alsoeen found to activate due to eye gaze contact (George, Driver, &olan, 2001), the mechanisms of these social effects also remain toe elucidated.

. Conclusion

Taken together, abundant evidence from neuropsychologicalnd neuroimaging studies indicate that spatial attention andwareness can be influenced by the affective and social significancef sensory stimuli. These findings indicate that attention and stim-lus awareness are not only controlled by frontoparietal networks,lassically associated with these functions, but also by limbic com-

onents such as the amygdala, orbitofrontal cortex, and perhapstriato-mesencephalic circuits. These limbic structures may eithernteract with fronto-parietal areas, directly with sensory areas suchs extrastriate visual cortex, or perhaps with both, in order to detect

chologia 50 (2012) 1054– 1071 1067

the affective and motivational value of stimuli and then act toprioritize orienting and awareness for those salient stimuli. Thishypothesis would accord with Mesulam’s model of attention, whichincluded a motivational component in neural networks controllingspatial attention, although the exact substrates of motivational pro-cesses were different in this model (Mesulam, 1981). Importantly,this proposal predicts at least partial independence between atten-tion mechanisms that are disrupted in neglect patients and emotionmechanisms that modulate perception.

Moreover, emotion effects on perception and awareness appearto operate in a largely reflexive and “implicit” manner, when emo-tional features are not directly relevant to the task. They can alsosubserve significant learning, as shown by recent experimentsusing pavlovian conditioning or reward learning. These aspects arepotentially useful for being exploited in rehabilitation settings, asprocedures based on implicit strategies, such as prism adaptation,might have a stronger and more generalized impact on neglectbehavior as compared with procedures based on explicit instruc-tions. These latter procedures tend to be learned “verbally” in therehabilitation sessions but less efficiently implemented in real lifeconditions. Yet, many questions still remain open regarding theneural substrates of these effects and the role of distinct affectivedimensions, e.g. in relation to the positive or negative valence ofstimuli.

Furthermore, it is important to recall that these emotion effectsmight be relatively weak and provide only partial biases coun-teracting neglect deficits. Thus, in most of the studies presentedabove, extinction remained significant despite the emotional facil-itation and therefore emotional stimuli do not fully override thepathological inattention towards the contralesional side. More-over, emotional effects might habituate after repeated exposure,while any useful exploitation for rehabilitation approaches ofneglect would require sustained efficacy. For instance, patient GKin our fMRI study (Vuilleumier, Armony, et al., 2002) detected fear-ful faces better than neutral faces only during the first and secondscan sessions, but not the third. Finally, the implicit effects of emo-tional cues might depend on the sparing of specific brain areas andthus also vary across different patients (Grandjean et al., 2008;Lucas & Vuilleumier, 2008), similarly as other preattentive pro-cesses that contribute to organize and select sensory information tomodulate competition weight in attention, but to different degreein different patients as a function of lesion extent (Vuilleumier,Valenza, et al., 2001). Further research in larger groups of patients isclearly needed in order to answer these questions. Finally, given thewell-known dominance of the right hemisphere for both attentionand emotion processes, further investigations should also addresswhether a partial recovery of neglect for emotional stimuli wouldalso be seen in left brain-damaged patients when, for instance,emotional faces or voices are presented in the right hemifield orhemispace.

In sum, the main conclusions drawn from these findings isthat emotion processes can directly gate and shape perception byenhancing sensory processing and thus bias competition for atten-tion selection. Such effects are not only observed in healthy controlsbut may be preserved in neglect patients despite their lesion, andthus appear reminiscent of some “pre-attentive” processes that stilloperate in the neglected field, such as object-based attention. Inthis sense, these effects constitute a distinct source of control onstimulus-awareness, which may be qualified of “emotion-basedattention” (Vuilleumier, 2005a) or “motivated attention” (Lang,Bradley, & Cuthbert, 1997), at least partly independent of top-down mechanisms of spatial attention mediated by frontal andparietal cortices. A better understanding of these mechanisms andtheir conditions of optimal operation seems to offer new per-

spectives to develop or improve therapeutic strategies in neglectpatients.

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cknowledgements

This work was supported by the Generalitat de Catalunya (Beat-iu de Pinós Postdoctoral Grant, 2009 BP-A 00117) to JDB, a grantf the Société Académique de Genève to PV, and a grant of theôpitaux Universitaires de Genève to AS.

eferences

glioti, S., Smania, N., Barbieri, C., & Corbetta, M. (1997). Influence of stimulussalience and attentional demands on visual search patterns in hemispatialneglect. Brain and Cognition, 34(3), 388–403.

kiyama, T., Kato, M., Muramatsu, T., Umeda, S., Saito, F., & Kashima, H. (2007).Unilateral amygdala lesions hamper attentional orienting triggered by gazedirection. Cerebral Cortex, 17(11), 2593–2600.

lorda, C., Serrano-Pedraza, I., Campos-Bueno, J. J., Sierra-Vazquez, V., & Montoya,P. (2007). Low spatial frequency filtering modulates early brain processing ofaffective complex pictures. Neuropsychologia, 45(14), 3223–3233.

maral, D. G., Bauman, M. D., Capitanio, J. P., Lavenex, P., Mason, W. A., Mauldin-Jourdain, M. L., et al. (2003). The amygdala: Is it an essential component of theneural network for social cognition? Neuropsychologia, 41(4), 517–522.

mting, J. M., Greening, S. G., & Mitchell, D. G. (2010). Multiple mechanisms ofconsciousness: The neural correlates of emotional awareness. Journal of Neu-roscience, 30(30), 10039–10047.

nders, S., Eippert, F., Wiens, S., Birbaumer, N., Lotze, M., & Wildgruber, D. (2009).When seeing outweighs feeling: A role for prefrontal cortex in passive controlof negative affect in blindsight. Brain, 132(Pt 11), 3021L 3031.

nderson, A. K., Christoff, K., Panitz, D., De Rosa, E., & Gabrieli, J. D. (2003). Neu-ral correlates of the automatic processing of threat facial signals. Journal ofNeuroscience, 23(13), 5627–5633.

nderson, A. K., & Phelps, E. A. (2001). Lesions of the human amygdala impairenhanced perception of emotionally salient events. Nature, 411(6835), 305–309.

ach, D. R., Talmi, D., Hurlemann, R., Patin, A., & Dolan, R. J. (2011). Automatic rele-vance detection in the absence of a functional amygdala. Neuropsychologia, 49(5),1302–1305.

ar, M. (2003). A cortical mechanism for triggering top-down facilitation in visualobject recognition. Journal of Cognitive Neuroscience, 15(4), 600–609.

ar, M., & Neta, M. (2007). Visual elements of subjective preference modulate amyg-dala activation. Neuropsychologia, 45(10), 2191–2200.

axter, M. G., & Murray, E. A. (2002). The amygdala and reward. Nature Reviews.Neuroscience, 3(7), 563–573.

aylis, G. C., Driver, J., Baylis, L. L., & Rafal, R. D. (1994). Reading of letters and wordsin a patient with Balint’s syndrome. Neuropsychologia, 32(10), 1273–1286.

eck, D. M., & Kastner, S. (2009). Top-down and bottom-up mechanisms in biasingcompetition in the human brain. Vision Research, 49(10), 1154–1165.

eck, D. M., Rees, G., Frith, C. D., & Lavie, N. (2001). Neural correlates of changedetection and change blindness. Nature Neuroscience, 4(6), 645–650.

ehrmann, M., Ebert, P., & Black, S. E. (2004). Hemispatial neglect and visual search:A large scale analysis. Cortex, 40(2), 247–263.

entley, P., Vuilleumier, P., Thiel, C. M., Driver, J., & Dolan, R. J. (2003). Cholinergicenhancement modulates neural correlates of selective attention and emotionalprocessing. Neuroimage, 20(1), 58–70.

enuzzi, F., Meletti, S., Zamboni, G., Calandra-Buonaura, G., Serafini, M., Lui, F., et al.(2004). Impaired fear processing in right mesial temporal sclerosis: A fMRI study.Brain Research Bulletin, 63(4), 269–281.

ermpohl, F., Pascual-Leone, A., Amedi, A., Merabet, L. B., Fregni, F., Gaab, N., et al.(2006). Dissociable networks for the expectancy and perception of emotionalstimuli in the human brain. Neuroimage, 30(2), 588–600.

erti, A., Oxbury, S., Oxbury, J., Affanni, P., Umilta, C., & Orlandi, L. (1999). Somatosen-sory extinction for meaningful objects in a patient with right hemispheric stroke.Neuropsychologia, 37(3), 333–343.

erti, A., & Rizzolatti, G. (1992). Visual processing without awareness: Evidence fromunilateral neglect. Journal of Cognitive Neuroscience, 4, 7.

indemann, M., Burton, A. M., Hooge, I. T., Jenkins, R., & de Haan, E. H. (2005). Facesretain attention. Psychonomic Bulletin and Review, 12(6), 1048–1053.

isiach, E., & Rusconi, M. L. (1990). Break-down of perceptual awareness in unilateralneglect. Cortex, 26(4), 643–649.

lue, V. L. (2010). And along came a spider: An attentional bias for the detection ofspiders in young children and adults. Journal of Experimental Child Psychology,107, 8.

ouret, S., & Richmond, B. J. (2010). Ventromedial and orbital prefrontal neuronsdifferentially encode internally and externally driven motivational values inmonkeys. Journal of Neuroscience, 30(25), 8591–8601.

ruce, V., & Young, A. (1986). Understanding face recognition. British Journal of Psy-chology, 77(Pt 3), 305–327.

ullier, J. (2001). Integrated model of visual processing. Brain Research. Brain ResearchReviews, 36(2–3), 96–107.

ullier, J., & Kennedy, H. (1983). Projection of the lateral geniculate nucleus onto

cortical area V2 in the macaque monkey. Experimental Brain Research, 53(1),168–172.

als, N., Devuyst, G., Afsar, N., Karapanayiotides, T., & Bogousslavsky, J. (2002). Puresuperficial posterior cerebral artery territory infarction in The Lausanne StrokeRegistry. Journal of Neurology, 249(7), 855–861.

chologia 50 (2012) 1054– 1071

Carretie, L., Hinojosa, J. A., Martin-Loeches, M., Mercado, F., & Tapia, M. (2004). Auto-matic attention to emotional stimuli: Neural correlates. Human Brain Mapping,22(4), 290–299.

Catani, M., Howard, R. J., Pajevic, S., & Jones, D. K. (2002). Virtual in vivo interac-tive dissection of white matter fasciculi in the human brain. Neuroimage, 17(1),77–94.

Catani, M., Jones, D. K., & Ffytche, D. H. (2005). Perisylvian language networks of thehuman brain. Annals of Neurology, 57(1), 8–16.

Cavada, C., Company, T., Tejedor, J., Cruz-Rizzolo, R. J., & Reinoso-Suarez, F. (2000).The anatomical connections of the macaque monkey orbitofrontal cortex. Areview. Cerebral Cortex, 10(3), 220–242.

Clarke, S., Riahi-Arya, S., Tardif, E., Eskenasy, A. C., & Probst, A. (1999). Thalamicprojections of the fusiform gyrus in man. European Journal of Neuroscience, 11(5),1835–1838.

Coelho, C. M., Cloete, S., & Wallis, G. (2010). The face-in-the-crowd effect: Whenangry faces are just cross(es). Journal of Vision, 10(1), 7, 1–14.

Cohen, M. A., Alvarez, G. A., & Nakayama, K. (2011). Natural-scene perceptionrequires attention. Psychological Science, 22(9), 1165–1172.

Committeri, G., Pitzalis, S., Galati, G., Patria, F., Pelle, G., Sabatini, U., et al. (2007).Neural bases of personal and extrapersonal neglect in humans. Brain, 130(Pt 2),431–441.

Corbetta, M., Kincade, M. J., Lewis, C., Snyder, A. Z., & Sapir, A. (2005). Neural basisand recovery of spatial attention deficits in spatial neglect. Nature Neuroscience,8(11), 1603–1610.

Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-drivenattention in the brain. Nature Reviews. Neuroscience, 3(3), 201–215.

Damasio, A. R., Damasio, H., & Chui, H. C. (1980). Neglect following damage to frontallobe or basal ganglia. Neuropsychologia, 18(2), 123–132.

Day-Brown, J. D., Wei, H., Chomsung, R. D., Petry, H. M., & Bickford, M. E. (2010). Pulv-inar projections to the striatum and amygdala in the tree shrew. Front Neuroanat,4, 143.

de Gelder, B., Morris, J. S., & Dolan, R. J. (2005). Unconscious fear influences emotionalawareness of faces and voices. Proceedings of the National Academy of Sciences ofthe United States of America, 102(51), 18682–18687.

de Gelder, B., Vroomen, J., Pourtois, G., & Weiskrantz, L. (1999). Non-conscious recog-nition of affect in the absence of striate cortex. Neuroreport, 10(18), 3759–3763.

Dehaene, S., Changeux, J. P., Naccache, L., Sackur, J., & Sergent, C. (2006). Conscious,preconscious, and subliminal processing: A testable taxonomy. Trends in Cogni-tive Sciences, 10(5), 204–211.

Dehaene, S., Naccache, L., Cohen, L., Bihan, D. L., Mangin, J. F., Poline, J. B., et al. (2001).Cerebral mechanisms of word masking and unconscious repetition priming.Nature Neuroscience, 4(7), 752–758.

Deouell, L. Y. (2002). Pre-requisites for conscious awareness: Clues from electro-physiological and behavioral studies of unilateral neglect patients. Consciousnessand Cognition, 11(4), 546–567.

Dering, B., Martin, C. D., Moro, S., Pegna, A. J., & Thierry, G. (2011). Face-sensitiveprocesses one hundred milliseconds after picture onset. Front Hum Neurosci, 5,93.

Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention.Annual Review of Neuroscience, 18, 193–222.

di Pellegrino, G., Rafal, R., & Tipper, S. P. (2005). Implicitly evoked actions modu-late visual selection: Evidence from parietal extinction. Current Biology, 15(16),1469–1472.

Di Russo, F., Aprile, T., Spitoni, G., & Spinelli, D. (2008). Impaired visual processingof contralesional stimuli in neglect patients: A visual-evoked potential study.Brain, 131(Pt 3), 842L 854.

Doricchi, F., & Angelelli, P. (1999). Misrepresentation of horizontal space in leftunilateral neglect: Role of hemianopia. Neurology, 52(9), 1845–1852.

Doricchi, F., & Tomaiuolo, F. (2003). The anatomy of neglect without hemi-anopia: A key role for parietal-frontal disconnection? Neuroreport, 14(17), 2239–2243.

Downing, P. E., Chan, A. W., Peelen, M. V., Dodds, C. M., & Kanwisher, N. (2006).Domain specificity in visual cortex. Cerebral Cortex, 16(10), 1453–1461.

Dringenberg, H. C., Saber, A. J., & Cahill, L. (2001). Enhanced frontal cortex activa-tion in rats by convergent amygdaloid and noxious sensory signals. Neuroreport,12(11), 2395–2398.

Driver, J. (1995). Object segmentation and visual neglect. Behavioural Brain Research,71(1–2), 135–146.

Driver, J., Baylis, G. C., & Rafal, R. D. (1992). Preserved figure-ground segregation andsymmetry perception in visual neglect. Nature, 360(6399), 73–75.

Driver, J., & Mattingley, J. B. (1998). Parietal neglect and visual awareness. NatureNeuroscience, 1(1), 17–22.

Driver, J., & Vuilleumier, P. (2001a). Perceptual awareness and its loss in unilateralneglect and extinction. Cognition, 79(1–2), 39–88.

Driver, J., & Vuilleumier, P. (2001b). Unconscious processing in neglect and extinc-tion. In B. De Gelder, E. H. F. De Haan, & C. A. Heywood (Eds.), Out of mind: Varietiesof unconscious processes (pp. 107–139). New York: Oxford University Press.

Driver, J., Vuilleumier, P., Eimer, M., & Rees, G. (2001). Functional magnetic resonanceimaging and evoked potential correlates of conscious and unconscious vision inparietal extinction patients. Neuroimage, 14(1 Pt 2), S68–S75.

Driver, J., Vuilleumier, P., & Husain, M. (2004). Spatial neglect and extinction. In

M. S. Gazzaniga (Ed.), The new cognitive neurosciences (3rd ed., pp. 589–606).Cambridge, MA: MIT Press.

Eastwood, J. D., Smilek, D., & Merikle, P. M. (2001). Differential attentional guidanceby unattended faces expressing positive and negative emotion. Perception andPsychophysics, 63(6), 1004–1013.

ropsy

E

E

E

E

F

F

F

F

F

F

F

F

F

F

G

G

G

G

G

G

G

G

G

H

H

H

H

H

H

H

H

J. Domínguez-Borràs et al. / Neu

imer, M. (2000). The face-specific N170 component reflects late stages in the struc-tural encoding of faces. Neuroreport, 11(10), 2319–2324.

imer, M., Maravita, A., Van Velzen, J., Husain, M., & Driver, J. (2002). The electro-physiology of tactile extinction: ERP correlates of unconscious somatosensoryprocessing. Neuropsychologia, 40(13), 2438–2447.

sterman, M., McGlinchey-Berroth, R., & Milberg, W. (2000). Preattentive and atten-tive visual search in individuals with hemispatial neglect. Neuropsychology,14(4), 599–611.

thofer, T., Bretscher, J., Gschwind, M., Kreifelts, B., Wildgruber, D., & Vuilleumier,P. (2011). Emotional voice areas: Anatomic location, functional properties, andstructural connections revealed by combined fMRI/DTI. Cerebral Cortex.

ecteau, S., Belin, P., Joanette, Y., & Armony, J. L. (2007). Amygdala responses tononlinguistic emotional vocalizations. Neuroimage, 36(2), 480–487.

lykt, A. (2005). Visual search with biological threat stimuli: Accuracy, reactiontimes, and heart rate changes. Emotion, 5(3), 349–353.

lykt, A., & Caldara, R. (2006). Tracking fear in snake and spider fearful participantsduring visual search: A multi-response domain study. Cognition and Emotion,20(8), 16.

ox, E. (2002a). Processing emotional facial expressions: The role of anxiety andawareness. Cognitive, Affective & Behavioral Neuroscience, 2(1), 52–63.

ox, E. (2002b). Processing of emotional facial expressions: The role of anxiety andawareness. Cognitive, Affective & Behavioral Neuroscience, 2(1), 52–63.

ox, E., Lester, V., Russo, R., Bowles, R. J., Pichler, A., & Dutton, K. (2000). Facialexpressions of emotion: Are angry faces detected more efficiently? Cognitionand Emotion, 14, 61–92.

reese, J. L., & Amaral, D. G. (2005). The organization of projections from the amygdalato visual cortical areas TE and V1 in the macaque monkey. Journal of ComparativeNeurology, 486(4), 295–317.

reese, J. L., & Amaral, D. G. (2006). Synaptic organization of projections from theamygdala to visual cortical areas TE and V1 in the macaque monkey. Journal ofComparative Neurology, 496(5), 655–667.

riedman, D. P., Murray, E. A., O’Neill, J. B., & Mishkin, M. (1986). Cortical connec-tions of the somatosensory fields of the lateral sulcus of macaques: Evidencefor a corticolimbic pathway for touch. Journal of Comparative Neurology, 252(3),323–347.

rischen, A., Bayliss, A. P., & Tipper, S. P. (2007). Gaze cueing of attention: Visual atten-tion, social cognition, and individual differences. Psychological Bulletin, 133(4),694–724.

affan, D., & Hornak, J. (1997). Visual neglect in the monkey. Representation anddisconnection. Brain, 120(Pt 9), 1647–1657.

allese, V., Keysers, C., & Rizzolatti, G. (2004). A unifying view of the basis of socialcognition. Trends in Cognitive Sciences, 8(9), 396–403.

eorge, N., Dolan, R. J., Fink, G. R., Baylis, G. C., Russell, C., & Driver, J. (1999). Contrastpolarity and face recognition in the human fusiform gyrus. Nature Neuroscience,2(6), 574–580.

eorge, N., Driver, J., & Dolan, R. J. (2001). Seen gaze-direction modulates fusiformactivity and its coupling with other brain areas during face processing. Neuroim-age, 13(6 Pt 1), 1102L 1112.

ilchrist, I. D., Humphreys, G. W., & Riddoch, M. J. (1996). Grouping and extinction:Evidence for low-level modulation of visual selection. Cognitive Neuropsychol-ogy, 1223–1249.

rabowska, A., Marchewka, A., Seniow, J., Polanowska, K., Jednorog, K., Krolicki,L., et al. (2011). Emotionally negative stimuli can overcome attentionaldeficits in patients with visuo-spatial hemineglect. Neuropsychologia, 49(12),3327–3337.

randjean, D., Sander, D., Lucas, N., Scherer, K. R., & Vuilleumier, P. (2008). Effectsof emotional prosody on auditory extinction for voices in patients with spatialneglect. Neuropsychologia, 46(2), 487–496.

randjean, D., Sander, D., Pourtois, G., Schwartz, S., Seghier, M. L., Scherer, K. R., et al.(2005). The voices of wrath: Brain responses to angry prosody in meaninglessspeech. Nature Neuroscience, 8(2), 145–146.

rüsser, O. J., & Landis, T. (1991). Visual agnosia and other disturbances of visualperception and cognition. London: MacMillan.

alligan, P. W., Fink, G. R., Marshall, J. C., & Vallar, G. (2003). Spatial cogni-tion: Evidence from visual neglect. Trends in Cognitive Sciences, 7(3), 125–133.

ansen, C. H., & Hansen, R. D. (1988). Finding the face in the crowd: An angersuperiority effect. Journal of Personality and Social Psychology, 54(6), 917–924.

eilman, K. M., & Valenstein, E. (1979). Mechanisms underlying hemispatial neglect.Annals of Neurology, 5(2), 166–170.

eilman, K. M., Watson, R. T., & Valenstein, E. (1985). Neglect and related disorders. InK. M. Heilman, & E. Valenstein (Eds.), Clinical neuropsychology. Oxford UniversityPress: New York.

ickey, C., Chelazzi, L., & Theeuwes, J. (2010). Reward guides vision when it’s yourthing: Trait reward-seeking in reward-mediated visual priming. PLoS One, 5(11),e14087.

illis, A. E., Newhart, M., Heidler, J., Barker, P. B., Herskovits, E. H., & Degaonkar,M. (2005). Anatomy of spatial attention: Insights from perfusion imaging andhemispatial neglect in acute stroke. Journal of Neuroscience, 25(12), 3161–3167.

illyard, S. A., & Anllo-Vento, L. (1998). Event-related brain potentials in the studyof visual selective attention. Proceedings of the National Academy of Sciences of

the United States of America, 95(3), 781–787.

irsch, J., DeLaPaz, R. L., Relkin, N. R., Victor, J., Kim, K., Li, T., et al. (1995). Illusory con-tours activate specific regions in human visual cortex: Evidence from functionalmagnetic resonance imaging. Proceedings of the National Academy of Sciences ofthe United States of America, 92(14), 6469–6473.

chologia 50 (2012) 1054– 1071 1069

Hornak, J., Bramham, J., Rolls, E. T., Morris, R. G., O’Doherty, J., Bullock, P. R.,et al. (2003). Changes in emotion after circumscribed surgical lesions of theorbitofrontal and cingulate cortices. Brain, 126(Pt 7), 1691L 1712.

Huang, Y. M., Baddeley, A., & Young, A. W. (2008). Attentional capture by emotionalstimuli is modulated by semantic processing. Journal of Experimental Psychology:Human Perception Performance, 34(2), 328–339.

Huang, Y. M., & Yeh, Y. Y. (2011). Why does a red snake in the grass capture yourattention? Emotion, 11(2), 224–232.

Husain, M., & Kennard, C. (1996). Visual neglect associated with frontal lobe infarc-tion. Journal of Neurology, 243(9), 652–657.

Husain, M., & Kennard, C. (1997). Distractor-dependent frontal neglect. Neuropsy-chologia, 35(6), 829–841.

Ikeda, T., & Hikosaka, O. (2003). Reward-dependent gain and bias of visual responsesin primate superior colliculus. Neuron, 39(4), 693–700.

Itier, R. J., & Taylor, M. J. (2004). N170 or N1? Spatiotemporal differences betweenobject and face processing using ERPs. Cerebral Cortex, 14(2), 132–142.

Johnson, M. H. (2011). Face processing as a brain adaptation at multiple timescales.Quarterly Journal of Experimental Psychology (Hove), 64(10), 1873–1888.

Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A modulein human extrastriate cortex specialized for face perception. Journal of Neuro-science, 17(11), 4302–4311.

Kanwisher, N., & Wojciulik, E. (2000). Visual attention: Insights from brain imaging.Nature Reviews. Neuroscience, 1(2), 91–100.

Karnath, H. O., Fruhmann Berger, M., Kuker, W., & Rorden, C. (2004). The anatomy ofspatial neglect based on voxelwise statistical analysis: A study of 140 patients.Cerebral Cortex, 14(10), 1164–1172.

Karnath, H. O., Rennig, J., Johannsen, L., & Rorden, C. (2011). The anatomy underlyingacute versus chronic spatial neglect: A longitudinal study. Brain, 134(Pt 3), 903L912.

Karnath, H. O., & Rorden, C. (2011). The anatomy of spatial neglect. Neuropsychologia.Karnath, H. O., Zopf, R., Johannsen, L., Fruhmann Berger, M., Nagele, T., & Klose, U.

(2005). Normalized perfusion MRI to identify common areas of dysfunction:Patients with basal ganglia neglect. Brain, 128(Pt 10), 2462L 2469.

Kastner, S., & Ungerleider, L. G. (2001). The neural basis of biased competition inhuman visual cortex. Neuropsychologia, 39(12), 1263–1276.

Kawasaki, H., Adolphs, R., Oya, H., Kovach, C., Damasio, H., Kaufman, O., et al. (2005).Analysis of single-unit responses to emotional scenes in human ventromedialprefrontal cortex. Journal of Cognitive Neuroscience, 17(10), 1509–1518.

Kawasaki, H., Kaufman, O., Damasio, H., Damasio, A. R., Granner, M., Bakken, H., et al.(2001). Single-neuron responses to emotional visual stimuli recorded in humanventral prefrontal cortex. Nature Neuroscience, 4(1), 15–16.

Kinsbourne, M. (1970). A model for the mechanism of unilateral neglect of space.Transactions of the American Neurological Association, 95, 143–146.

Kinsbourne, M. (1977). Hemi-neglect and hemispheric rivalry. In E. A. Weinstein, &R. P. Friedland (Eds.), Advances in neurology (pp. 41–49). New York: Raven Press.

Kleinke, C. L. (1986). Gaze and eye contact: A research review. Psychological Bulletin,100(1), 78–100.

Koch, G., Oliveri, M., Cheeran, B., Ruge, D., Lo Gerfo, E., Salerno, S., et al. (2008).Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. Brain, 131(Pt 12), 3147–3155.

Kristjansson, A., Vuilleumier, P., Malhotra, P., Husain, M., & Driver, J. (2005). Primingof color and position during visual search in unilateral spatial neglect. Journal ofCognitive Neuroscience, 17(6), 859–873.

Kumral, E., Kocaer, T., Ertubey, N. O., & Kumral, K. (1995). Thalamic hemorrhage. Aprospective study of 100 patients. Stroke, 26(6), 964–970.

Ladavas, E., Menghini, G., & Umilta, C. (1994). A rehabilitation study of hemispatialneglect. Cognitive Neuropsychology, 11(1), 75–95.

Lamme, V. A. (2003). Why visual attention and awareness are different. Trends inCognitive Sciences, 7(1), 12–18.

Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). Motivated attention: Affect,activation and action. In P. J. Lang, R. F. Simons, & M. F. Balaban (Eds.), Atten-tion and orienting: Sensory and motivational processes (pp. 97–135). Hillsdale, NJ:Lawrence Erlbaum Associates.

Langton, S. R. H., Law, A. S., Burton, A. M., & Schweinberger, S. R. (2008). Attentioncapture by faces. Cognition, 107(1), 330–342.

LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23,155–184.

Leibovitch, F. S., Black, S. E., Caldwell, C. B., Ebert, P. L., Ehrlich, L. E., & Szalai, J. P.(1998). Brain-behavior correlations in hemispatial neglect using CT and SPECT:The Sunnybrook Stroke Study. Neurology, 50(4), 901–908.

Levenson, R. W. (2003). Blood, sweat, and fears: The autonomic architecture ofemotion. Annals of the New York Academy of Sciences, 1000, 348–366.

Lhermitte, F., Turell, E., LeBrigand, D., & Chain, F. (1985). Unilateral visual neglect andwave P 300. A study of nine cases with unilateral lesions of the parietal lobes.Archives of Neurology, 42(6), 567–573.

Liu, J., Harris, A., & Kanwisher, N. (2002). Stages of processing in face perception: AnMEG study. Nature Neuroscience, 5(9), 910–916.

Lucas, N., Sch, S., Diserens, K., Leroy, R., Krattinger, S., & Vuilleumier, P. (2005).Gambling against neglect: Modulation of spatial attention by implicit rewardlearning. Journal of Cognitive Neuroscience, 151.

Lucas, N., & Vuilleumier, P. (2008). Effects of emotional and non-emotional cues on

visual search in neglect patients: Evidence for distinct sources of attentionalguidance. Neuropsychologia.

Luck, S. J., & Hillyard, S. A. (1994). Electrophysiological correlates of feature analysisduring visual search. Psychophysiology, 31(3), 291–308.

Mack, A., & Rock, I. (1998). Inattentional blindness. Cambridge, MA: MIT Press.

1 ropsy

M

M

M

M

M

M

M

M

M

N

N

O

O

O

O

P

P

P

P

P

P

P

P

P

P

P

P

P

P

P

R

RR

070 J. Domínguez-Borràs et al. / Neu

aravita, A., Posteraro, L., Husain, M., Vuilleumier, P., Schwartz, S., & Driver, J. (2007).Looking at human eyes affects contralesional stimulus processing after righthemispheric stroke. Neurology, 69(16), 1619–1621.

arshall, J. C., & Halligan, P. W. (1988). Blindsight and insight in visuo-spatial neglect.Nature, 336(6201), 766–767.

arzi, C. A., Girelli, M., Miniussi, C., Smania, N., & Maravita, A. (2000). Electrophys-iological correlates of conscious vision: Evidence from unilateral extinction.Journal of Cognitive Neuroscience, 12(5), 869–877.

attingley, J. B., Davis, G., & Driver, J. (1997). Preattentive filling-in of visual surfacesin parietal extinction. Science, 275(5300), 671–674.

aunsell, J. H. (2004). Neuronal representations of cognitive state: Reward or atten-tion? Trends in Cognitive Sciences, 8(6), 261–265.

esulam, M. M. (1981). A cortical network for directed attention and unilateralneglect. Annals of Neurology, 10(4), 309–325.

orand, S., Thut, G., de Peralta, R. G., Clarke, S., Khateb, A., Landis, T., et al. (2000).Electrophysiological evidence for fast visual processing through the humankoniocellular pathway when stimuli move. Cerebral Cortex, 10(8), 817–825.

orris, J. S., Ohman, A., & Dolan, R. J. (1999). A subcortical pathway to the rightamygdala mediating unseen fear. Proceedings of the National Academy of Sciencesof the United States of America, 96(4), 1680–1685.

ort, D. J., Malhotra, P., Mannan, S. K., Rorden, C., Pambakian, A., Kennard, C., et al.(2003). The anatomy of visual neglect. Brain, 126(Pt 9), 1986L 1997.

ieuwenhuys, R., Voogd, J., & Huihzen, C. (1988). The human central nervous system:A synopsis and atlas. Heidelberg: Springer-Verlag.

ummenmaa, L., & Calder, A. J. (2009). Neural mechanisms of social attention. Trendsin Cognitive Sciences, 13(3), 135–143.

’Craven, K. M., Downing, P. E., & Kanwisher, N. (1999). fMRI evidence for objects asthe units of attentional selection. Nature, 401(6753), 584–587.

hman, A., Flykt, A., & Esteves, F. (2001). Emotion drives attention: Detecting thesnake in the grass. Journal of Experimental Psychology: General, 130(3), 466–478.

hman, A., Lundqvist, D., & Esteves, F. (2001). The face in the crowd revisited: Athreat advantage with schematic stimuli. Journal of Personality and Social Psy-chology, 80(3), 381–396.

kada, T., Sato, W., Kubota, Y., Usui, K., Inoue, Y., Murai, T., et al. (2008). Involve-ment of medial temporal structures in reflexive attentional shift by gaze. SocialCognitive and Affective Neuroscience, 3(1), 80–88.

avlovskaya, M., Ring, H., Groswasser, Z., & Hochstein, S. (2002). Searching withunilateral neglect. Journal of Cognitive Neuroscience, 14(5), 745–756.

eelen, M. V., Atkinson, A. P., Andersson, F., & Vuilleumier, P. (2007). Emotional mod-ulation of body-selective visual areas. Social Cognitive and Affective Neuroscience,2, 274–283.

eelen, M. V., & Downing, P. E. (2005). Selectivity for the human body in the fusiformgyrus. Journal of Neurophysiology, 93(1), 603–608.

egna, A. J., Khateb, A., Lazeyras, F., & Seghier, M. L. (2005). Discriminating emo-tional faces without primary visual cortices involves the right amygdala. NatureNeuroscience, 8(1), 24–25.

essoa, L., & Adolphs, R. (2010). Emotion processing and the amygdala: From a‘low road’ to ‘many roads’ of evaluating biological significance. Nature Reviews.Neuroscience, 11(11), 773–783.

eyrin, C., Michel, C. M., Schwartz, S., Thut, G., Seghier, M., Landis, T., et al. (2010). Theneural substrates and timing of top-down processes during coarse-to-fine cate-gorization of visual scenes: A combined fMRI and ERP study. Journal of CognitiveNeuroscience, 22(12), 2768–2780.

iech, R. M., McHugo, M., Smith, S. D., Dukic, M. S., Van Der Meer, J., Abou-Khalil, B.,et al. (2011). Attentional capture by emotional stimuli is preserved in patientswith amygdala lesions. Neuropsychologia, 49(12), 3314–3319.

itzalis, S., Spinelli, D., & Zoccolotti, P. (1997). Vertical neglect: Behavioral and elec-trophysiological data. Cortex, 33(4), 679–688.

latt, M. L., & Glimcher, P. W. (1999). Neural correlates of decision variables inparietal cortex. Nature, 400(6741), 233–238.

leger, B., Blankenburg, F., Ruff, C. C., Driver, J., & Dolan, R. J. (2008). Reward facilitatestactile judgments and modulates hemodynamic responses in human primarysomatosensory cortex. Journal of Neuroscience, 28(33), 8161–8168.

ourtois, G., Grandjean, D., Sander, D., & Vuilleumier, P. (2004). Electrophysiologicalcorrelates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14(6),619–633.

ourtois, G., Spinelli, L., Seeck, M., & Vuilleumier, P. (2010). Temporal precedenceof emotion over attention modulations in the lateral amygdala: IntracranialERP evidence from a patient with temporal lobe epilepsy. Cognitive, Affective& Behavioral Neuroscience, 10(1), 83–93.

ourtois, G., Thut, G., Grave de Peralta, R., Michel, C., & Vuilleumier, P. (2005).Two electrophysiological stages of spatial orienting towards fearful faces: Earlytemporo-parietal activation preceding gain control in extrastriate visual cortex.Neuroimage, 26(1), 149–163.

urcell, D. G., & Stewart, A. L. (2010). Still another confounded face in the crowd.Attention, Perception and Psychophysics, 72(8), 2115–2127.

urcell, D. G., Stewart, A. L., & Skov, R. B. (1996). It takes a confounded face to popout of a crowd. Perception, 25(9), 1091–1108.

afal, R., Danziger, S., Grossi, G., Machado, L., & Ward, R. (2002). Visual detectionis gated by attending for action: Evidence from hemispatial neglect. Proceed-ings of the National Academy of Sciences of the United States of America, 99(25),

16371–16375.

afal, R. D. (1994). Neglect. Current Opinion in Neurobiology, 4, 231–236.afal, R. D., & Posner, M. I. (1987). Deficits in human visual spatial attention following

thalamic lesions. Proceedings of the National Academy of Sciences of the UnitedStates of America, 84(20), 7349–7353.

chologia 50 (2012) 1054– 1071

Rappaport, S. J., Riddoch, M. J., & Humphreys, G. W. (2011). The grouping bene-fit in extinction: Overcoming the temporal order bias. Neuropsychologia, 49(1),151–155.

Rauss, K., Pourtois, G., Vuilleumier, P., & Schwartz, S. (2011). Effects of attentionalload on early visual processing depend on stimulus timing. Human Brain Map-ping.

Rees, G. (2007). Neural correlates of the contents of visual awareness in humans.Philosophical Transactions of the Royal Society of London, Series B: Biological Sci-ences, 362(1481), 877–886.

Rees, G., Wojciulik, E., Clarke, K., Husain, M., Frith, C., & Driver, J. (2000). Unconsciousactivation of visual cortex in the damaged right hemisphere of a parietal patientwith extinction. Brain, 123(Pt 8), 1624–1633.

Rees, G., Wojciulik, E., Clarke, K., Husain, M., Frith, C., & Driver, J. (2002). Neuralcorrelates of conscious and unconscious vision in parietal extinction. Neurocase,8(5), 387–393.

Richards, A., & Blanchette, I. (2004). Independent manipulation of emotion inan emotional stroop task using classical conditioning. Emotion, 4(3), 275–281.

Riddoch, M. J., Humphreys, G. W., Edwards, S., Baker, T., & Willson, K. (2003). See-ing the action: Neuropsychological evidence for action-based effects on objectselection. Nature Neuroscience, 6(1), 82–89.

Ristic, J., Wright, A., & Kingstone, A. (2007). Attentional control and reflexive orient-ing to gaze and arrow cues. Psychonomic Bulletin and Review, 14(5), 964–969.

Robertson, I. H., Mattingley, J. B., Rorden, C., & Driver, J. (1998). Phasic alerting ofneglect patients overcomes their spatial deficit in visual awareness. Nature,395(6698), 169–172.

Robertson, L. C., Eglin, M., & Knight, R. (2003). Grouping influences in unilateralvisual neglect. Journal of Clinical and Experimental Neuropsychology, 25(3), 297–307.

Rorden, C., Fruhmann Berger, M., & Karnath, H. O. (2006). Disturbed line bisection isassociated with posterior brain lesions. Brain Research, 1080(1), 17–25.

Rotshtein, P., Richardson, M. P., Winston, J. S., Kiebel, S. J., Vuilleumier, P., Eimer, M.,et al. (2010). Amygdala damage affects event-related potentials for fearful facesat specific time windows. Human Brain Mapping, 31(7), 1089–1105.

Sabatinelli, D., Fortune, E. E., Li, Q., Siddiqui, A., Krafft, C., Oliver, W. T., et al. (2011).Emotional perception: Meta-analyses of face and natural scene processing. Neu-roimage, 54(3), 2524–2533.

Sabatinelli, D., Lang, P. J., Bradley, M. M., Costa, V. D., & Keil, A. (2009). The timing ofemotional discrimination in human amygdala and ventral visual cortex. Journalof Neuroscience, 29(47), 14864–14868.

Saj, A., Verdon, V., Vocat, R., & Vuilleumier, P. (2011). ‘The anatomy underlying acuteversus chronic spatial neglect’ also depends on clinical tests. Brain.

Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved systemfor relevance detection. Reviews in the Neurosciences, 14(4), 303–316.

Sarri, M., Blankenburg, F., & Driver, J. (2006). Neural correlates of crossmodalvisual-tactile extinction and of tactile awareness revealed by fMRI in a right-hemisphere stroke patient. Neuropsychologia, 44(12), 2398–2410.

Sarter, M., Hasselmo, M. E., Bruno, J. P., & Givens, B. (2005). Unraveling the attentionalfunctions of cortical cholinergic inputs: Interactions between signal-driven andcognitive modulation of signal detection. Brain Research. Brain Research Reviews,48(1), 98–111.

Schmid, M. C., Mrowka, S. W., Turchi, J., Saunders, R. C., Wilke, M., Peters, A. J., et al.(2010). Blindsight depends on the lateral geniculate nucleus. Nature, 466(7304),373–377.

Schmolesky, M. T., Wang, Y., Hanes, D. P., Thompson, K. G., Leutgeb, S., Schall, J.D., et al. (1998). Signal timing across the macaque visual system. Journal ofNeurophysiology, 79(6), 3272–3278.

Schubo, A., Gendolla, G. H., Meinecke, C., & Abele, A. E. (2006). Detecting emotionalfaces and features in a visual search paradigm: Are faces special? Emotion, 6(2),246–256.

Shipp, S. (2003). The functional logic of cortico-pulvinar connections. PhilosophicalTransactions of the Royal Society of London, Series B: Biological Sciences, 358(1438),1605–1624.

Shomstein, S., Kimchi, R., Hammer, M., & Behrmann, M. (2010). Perceptual group-ing operates independently of attentional selection: Evidence from hemispatialneglect. Attention, Perception and Psychophysics, 72(3), 607–618.

Smania, N., Martini, M. C., Prior, M., & Marzi, C. A. (1996). Input and response deter-minants of visual extinction: A case study. Cortex, 32(4), 567–591.

Smilek, D., Frischen, A., Reynolds, M. G., Gerritsen, C., & Eastwood, J. D. (2007).What influences visual search efficiency? Disentangling contributions of preat-tentive and postattentive processes. Perception and Psychophysics, 69(7), 1105–1116.

Soto, D., Funes, M. J., Guzman-Garcia, A., Warbrick, T., Rotshtein, P., & Humphreys,G. W. (2009). Pleasant music overcomes the loss of awareness in patients withvisual neglect. Proceedings of the National Academy of Sciences of the United Statesof America, 106(14), 6011–6016.

Spinelli, D., & Di Russo, F. (1996). Visual evoked potentials are affected by trunkrotation in neglect patients. Neuroreport, 7(2), 553–556.

Stolarova, M., Keil, A., & Moratti, S. (2006). Modulation of the C1 visual event-related component by conditioned stimuli: Evidence for sensory plasticity inearly affective perception. Cerebral Cortex, 16(6), 876–887.

Sugase, Y., Yamane, S., Ueno, S., & Kawano, K. (1999). Global and fine informa-tion coded by single neurons in the temporal visual cortex. Nature, 400(6747),869–873.

Tamietto, M., & de Gelder, B. (2010). Neural bases of the non-conscious perceptionof emotional signals. Nature Reviews. Neuroscience, 11(10), 697–709.

ropsy

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T

T

T

T

T

T

V

V

V

V

V

V

V

V

V

V

V

V

V

V

V

V

J. Domínguez-Borràs et al. / Neu

amietto, M., Geminiani, G., Genero, R., & de Gelder, B. (2007). Seeing fearful bodylanguage overcomes attentional deficits in patients with neglect. Journal of Cog-nitive Neuroscience, 19(3), 445–454.

arkka, I. M., Luukkainen-Markkula, R., Pitkanen, K., & Hamalainen, H. (2011). Alter-ations in visual and auditory processing in hemispatial neglect: An evokedpotential follow-up study. International Journal of Psychophysiology, 79(2),272–279.

hiebaut de Schotten, M., Dell’acqua, F., Forkel, S. J., Simmons, A., Vergani, F., Murphy,D. G., et al. (2011). A lateralized brain network for visuospatial attention. NatureNeuroscience, 14(10), 1245–1246.

hiebaut de Schotten, M., Urbanski, M., Duffau, H., Volle, E., Levy, R., Dubois, B.,et al. (2005). Direct evidence for a parietal-frontal pathway subserving spatialawareness in humans. Science, 309(5744), 2226–2228.

ong, F., Nakayama, K., Vaughan, J. T., & Kanwisher, N. (1998). Binocular rivalryand visual awareness in human extrastriate cortex. Neuron, 21(4), 753–759.

reisman, A. (1982). Perceptual grouping and attention in visual search for fea-tures and for objects. Journal of Experimental Psychology: Human Perception andPerformance, 8(2), 194–214.

reisman, A., & Souther, J. (1985). Search asymmetry: A diagnostic for preatten-tive processing of separable features. Journal of Experimental Psychology: General,114(3), 285–310.

alenza, N., Seghier, M. L., Schwartz, S., Lazeyras, F., & Vuilleumier, P. (2004). Tactileawareness and limb position in neglect: Functional magnetic resonance imaging.Annals of Neurology, 55(1), 139–143.

allar, G., & Perani, D. (1986). The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man.Neuropsychologia, 24(5), 609–622.

anRullen, R., & Thorpe, S. J. (2002). Surfing a spike wave down the ventral stream.Vision Research, 42(23), 2593–2615.

erdon, V., Schwartz, S., Lovblad, K. O., Hauert, C. A., & Vuilleumier, P. (2010). Neu-roanatomy of hemispatial neglect and its functional components: A study usingvoxel-based lesion-symptom mapping. Brain, 133(Pt 3), 880L 894.

erleger, R., Heide, W., Butt, C., Wascher, E., & Kompf, D. (1996). On-line brainpotential correlates of right parietal patients’ attentional deficit. Electroen-cephalography and Clinical Neurophysiology, 99(5), 444–457.

rticka, P., Sander, D., & Vuilleumier, P. (2011). Effects of emotion regulation strategyon brain responses to the valence and social content of visual scenes. Neuropsy-chologia, 49(5), 1067–1082.

uilleumier, P. (2000). Faces call for attention: Evidence from patients with visualextinction. Neuropsychologia, 38(5), 693–700.

uilleumier, P. (2002). Perceived gaze direction in faces and spatial attention: Astudy in patients with parietal damage and unilateral neglect. Neuropsychologia,40(7), 1013–1026.

uilleumier, P. (2005a). How brains beware: Neural mechanisms of emotional atten-tion. Trends in Cognitive Sciences, 9(12), 585–594.

uilleumier, P. (2005b). Visual extinction and hemispatial neglect after brain dam-age: Neurophysiological basis of residual processing. In L. Itti, G. Rees, & J. K.Tsotsos (Eds.), Neurobiology of attention (pp. 351–357). San Diego: Elsevier.

uilleumier, P. (2007). Hemispatial neglect. In O. Godefroy, & J. Bogousslavsky (Eds.),Behavioral neurology in acute stroke management (pp. 148–197). Cambridge Uni-versity Press.

uilleumier, P. (2009). Attention and emotion. In D. Sander, & K. Scherer (Eds.),Emotion and the affective sciences (pp. 54–58). Oxford, UK: Oxford UniversityPress.

uilleumier, P., Armony, J. L., Clarke, K., Husain, M., Driver, J., & Dolan, R. J. (2002).Neural response to emotional faces with and without awareness: Event-relatedfMRI in a parietal patient with visual extinction and spatial neglect. Neuropsy-chologia, 40(12), 2156–2166.

uilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001). Effects of attention andemotion on face processing in the human brain: An event-related fMRI study.Neuron, 30(3), 829–841.

uilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2003). Distinct spatial fre-

quency sensitivities for processing faces and emotional expressions. NatureNeuroscience, 6(6), 624–631.

uilleumier, P., & Brosch, T. (2009). Interactions of emotion and attention in per-ception. In M. S. Gazzaniga (Ed.), The cognitive neurosciences IV (pp. 925–934).Cambridge, MA: MIT Press.

chologia 50 (2012) 1054– 1071 1071

Vuilleumier, P., & Driver, J. (2007). Modulation of visual processing by attention andemotion: Windows on causal interactions between human brain regions. Philo-sophical Transactions of the Royal Society of London, Series B: Biological Sciences,362(1481), 837–855.

Vuilleumier, P., Henson, R. N., Driver, J., & Dolan, R. J. (2002). Multiple levels of visualobject constancy revealed by event-related fMRI of repetition priming. NatureNeuroscience, 5(5), 491–499.

Vuilleumier, P., Hester, D., Assal, G., & Regli, F. (1996). Unilateral spatial neglectrecovery after sequential strokes. Neurology, 46(1), 184–189.

Vuilleumier, P., & Huang, Y. (2009). Emotional attention: Uncovering the mecha-nisms of affective biases in perception. Current Directions in Psychological Science,18(3), 148–152.

Vuilleumier, P., & Landis, T. (1998). Illusory contours and spatial neglect. Neuroreport,9(11), 2481–2484.

Vuilleumier, P., & Pourtois, G. (2007). Distributed and interactive brain mechanismsduring emotion face perception: Evidence from functional neuroimaging. Neu-ropsychologia, 45(1), 174–194.

Vuilleumier, P., & Rafal, R. D. (2000). A systematic study of visual extinction.Between- and within-field deficits of attention in hemispatial neglect. Brain,123(Pt 6), 1263–1279.

Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J., & Dolan, R. J. (2004). Distantinfluences of amygdala lesion on visual cortical activation during emotional faceprocessing. Nature Neuroscience, 7(11), 1271–1278.

Vuilleumier, P., & Sagiv, N. (2001). Two eyes make a pair: Facial organization and per-ceptual learning reduce visual extinction. Neuropsychologia, 39(11), 1144–1149.

Vuilleumier, P., Sagiv, N., Hazeltine, E., Poldrack, R. A., Swick, D., Rafal, R. D., et al.(2001). Neural fate of seen and unseen faces in visuospatial neglect: A combinedevent-related functional MRI and event-related potential study. Proceedings ofthe National Academy of Sciences of the United States of America, 98(6), 3495–3500.

Vuilleumier, P., & Schwartz, S. (2001a). Beware and be aware: Capture of spatialattention by fear-related stimuli in neglect. Neuroreport, 12(6), 1119–1122.

Vuilleumier, P., & Schwartz, S. (2001b). Emotional facial expressions capture atten-tion. Neurology, 56(2), 153–158.

Vuilleumier, P., Schwartz, S., Clarke, K., Husain, M., & Driver, J. (2002). Testing mem-ory for unseen visual stimuli in patients with extinction and spatial neglect.Journal of Cognitive Neuroscience, 14(6), 875–886.

Vuilleumier, P., Schwartz, S., Verdon, V., Maravita, A., Hutton, C., Husain, M.,et al. (2008). Abnormal attentional modulation of retinotopic cortex in parietalpatients with spatial neglect. Current Biology, 18(19), 1525–1529.

Vuilleumier, P., Valenza, N., & Landis, T. (2001). Explicit and implicit perception ofillusory contours in unilateral spatial neglect: Behavioural and anatomical cor-relates of preattentive grouping mechanisms. Neuropsychologia, 39(6), 597–610.

Ward, R., & Goodrich, S. (1996). Differences between objects and nonobjects in visualextinction: A competition for attention. Psychological Science, 7, 177–180.

Ward, R., Goodrich, S., & Driver, J. (1994). Grouping reduces visual extinction: Neu-ropsychological evidence for weight-linkage in visual selection. Visual Cognition,1, 101–129.

Weldon, D. A., DiNieri, J. A., Silver, M. R., Thomas, A. A., & Wright, R. E. (2007).Reward-related neuronal activity in the rat superior colliculus. Behavioural BrainResearch, 177(1), 160–164.

Whalen, P. J. (2007). The uncertainty of it all. Trends in Cognitive Sciences, 11(12),499–500.

Whalen, P. J., Kagan, J., Cook, R. G., Davis, F. C., Kim, H., Polis, S., et al. (2004). Humanamygdala responsivity to masked fearful eye whites. Science, 306(5704), 2061.

Williams, M. A., & Mattingley, J. B. (2004). Unconscious perception of non-threatening facial emotion in parietal extinction. Experimental Brain Research,154(4), 403–406.

Williams, M. A., Moss, S. A., Bradshaw, J. L., & Mattingley, J. B. (2005). Look at me, I’msmiling: Visual search for threatening and nonthreatening facial expressions.Visual Cognition, 12(1), 29–50.

Yamasaki, H., LaBar, K. S., & McCarthy, G. (2002). Dissociable prefrontal brain systemsfor attention and emotion. Proceedings of the National Academy of Sciences of theUnited States of America, 99(17), 11447–11451.

Yukie, M., & Iwai, E. (1981). Direct projection from the dorsal lateral geniculatenucleus to the prestriate cortex in macaque monkeys. Journal of ComparativeNeurology, 201, 81–97.

Zhang, W., & Luck, S. J. (2009). Feature-based attention modulates feedforward visualprocessing. Nature Neuroscience, 12(1), 24–25.