The cortical network for eye–hand coordination and … › meetings › 2007 › oct-nov ›...

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Neuropsychologia 44 (2006) 2607–2620

The cortical network for eye–hand coordination and its relevance tounderstanding motor disorders of parietal patients

Alexandra Battaglia-Mayer, Philippe S. Archambault, Roberto Caminiti ∗Dipartimento di Fisiologia umana e Farmacologia, Universita degli Studi di Roma “La Sapienza”, Piazzale Aldo Moro 5, 00185 Rome, Italy

Received 18 November 2005; accepted 29 November 2005Available online 2 February 2006

bstract

Cortical neurons in both superior (SPL) and inferior (IPL) parietal lobules are modulated by a variety of signals concerning planning andxecution of eye and hand movement. Thanks to these properties, parietal neurons are ideally suited for eye–hand coordination during reaching.n SPL, a fundamental feature of neurons is the invariance of their directional tuning properties across tasks that require different forms of spatialelationships between the eye and the hand. In such conditions, the orientation of the preferred directions (PDs) of individual SPL cells clusterithin a limited sector of space, the global tuning field (GTF), to be regarded as an ideal frame to dynamically match eye and hand signals on theasis of the orientation of their PDs. At the population level, the mean vectors of the GTF cover the direction continuum in a uniform fashion. Theseeurons are part of a parietal network richly interconnected with the premotor and motor areas of the frontal lobe. Thus, the reaching disordersf patients with optic ataxia might be interpreted as a consequence of the breakdown of the combinatorial mechanisms of the GTF of parietaleurons, and of their interplay with premotor cortex. In IPL, the main feature of eye and/or hand related neurons is the uneven distribution of their
Ds, that mostly point toward the contralateral space. This anisotropy of the representation of directional motor space might explain the movementisorders that characterize directional hypokinesia in neglect patients. In conclusion, the study of the dynamic properties of parietal neurons andf their relationships with the premotor cortex via cortico-cortical connections provides a basis for an interpretation of movement disorders ofarietal patients from a neurophysiological perspective.
2005 Elsevier Ltd. All rights reserved.

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eywords: Parietal cortex; Reaching; Eye–hand coordination; Optic ataxia; Di

. The functional architecture of the cortical networkor visual reaching

In the cerebral cortex, reaching to visual targets is encodedithin a distributed system including different parietal and

rontal areas. These are linked by association connections thatre always reciprocal. Therefore, when interpreting the opera-ions performed by any given cortical area, one cannot ignore theunctional repertoire and the dynamic mechanisms occurring inther nodes of the network. The parietal lobe receives, amongther signals, visual information from the extrastriate areas ofhe occipital lobe, and is reciprocally connected to the cortical
utput-areas of the frontal lobe, namely the premotor and motorortices. Therefore, the posterior parietal cortex (PPC) can beonsidered as an early and intermediate stage in the process lead-
∗ Corresponding author. Tel.: +39 06 4991 0967; fax: +39 06 4991 0942.E-mail address: [email protected] (R. Caminiti).

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028-3932/$ – see front matter © 2005 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2005.11.021

nal hypokinesia

ng from vision to movement. This applies to both the superiorSPL) and inferior (IPL) parietal lobules. In fact, the traditionalubdivision of PPC into SPL and IPL, regarded as higher-orderssociation areas in the respective domains of somesthesiand vision, is not tenable anymore. Both SPL and IPL receive,reat, and combine somatosensory and visual information, andse them for the composition of motor commands (for reviewsee Andersen & Buneo, 2002; Battaglia-Mayer, Caminiti,acquaniti, & Zago, 2003). Within both SPL and IPL, differentortical areas, identified on the basis of their functional reper-oire and cortico-cortical connections, operate on a multiplicityf signals (visual, somatosensory, auditory, vestibular, atten-ional, etc.), each of which influence cell activity with differenttrength, depending on the area considered. In the case of visualeaching, this combination of information in parietal cortex is
ot only confined to information of different modalities, but alsoefers to signals related to different effectors, such as the eye andhe hand (Mascaro, Battaglia-Mayer, Nasi, Amit, & Caminiti,003). Therefore, we believe that parietal cortex subserves

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he early stages of eye–hand coordination necessary for anyuccessful reach, under a variety of experimental conditions.

When the functional organization of the parietal and frontalreas is contrasted with their pattern of cortico-cortical con-ections, a reciprocal distributed system emerges (Fig. 1). Thisetwork is characterized by gradients of functional propertieslong the tangential dimensions of the cortex. The gradient-likerchitecture refers to the arrangement of visual, eye, and hand-elated signals. This aspect has been studied in a quantitativeashion in SPL and in the frontal cortex (Battaglia-Mayer et al.,001; Johnson, Ferraina, Bianchi, & Caminiti, 1996). At the cau-al and rostral poles of the network, respectively in the parietalareas V6A, 7 m) and in the dorso-rostral premotor (area PMdrr F7) cortex, eye signals predominate on coexisting hand infor-ation; on the contrary, hand information dominates eye signals

n the rostralmost part of the parietal cortex (areas PE), and inhe caudalmost part of the frontal cortex (PMdc or F2, MI); atntermediate levels in both the parietal (areas MIP, PEc, PEa)nd frontal (F2/M1 border) lobes, eye and hand signals coexist,ith different strength relationships depending on the cortical

rea considered. Similar trends of properties have been describedn the frontal node of the parieto-frontal network, across motorortex, pre-SMA and SMA (Alexander & Crutcher, 1990; Hoshi

Tanji, 2004; Matsuzaka, Aizawa, & Tanji, 1992; Rizzolatti etl., 1990). Throughout the network all these reach-related sig-als are directional in nature.

Superimposed on this functional dimension is a second one,elated to the type of information treated in the network. Movingrom caudal to rostral in SPL, a transition from preparatory (set-

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ig. 1. The parieto-frontal network for reaching. Main ipsilateral connections (arrowsn macaque monkeys are delimited according to the parcellations proposed by Pandy992) for the agranular frontal areas, and by Strick (see Picard & Strick, 1996) for thet al. (1996), Matelli et al. (1998), Marconi et al. (2001). Colours distinguish differ, lateral and medial views of the hemisphere, respectively. C, lateral view of the h

Galletti, Fattori, Battaglini, Shipp, & Zeki, 1996) to show the location of the areashe parieto-occipital sulcus. D, enlargement of the parietal region around the intrapar

edial and lateral banks of the IPS.

hologia 44 (2006) 2607–2620

nd memory-related) to movement signals occurs; the opposites true in the frontal cortex. Cells encoding eye and/or handosition information are ubiquitous at all tangential locationsf the network, so as to form a matrix on which preparatory andovement-related signal are embedded, and eventually selected

n the basis of task demands (Battaglia-Mayer et al., 2001;ohnson et al., 1996). This is not surprising if one considershat information about eye and hand position is essential underirtually all conditions for early planning of combined eye–handovements, such as those typical of reaching to visual targets.

n fact, if the modulation exerted by eye position on visualarietal neurons (for a review see Andersen & Buneo, 2002)avours the transformation of target location from retinal toody-centred coordinated, hand position signals are essential toompute hand movement trajectory. As such, they exert a pro-ound influence on encoding movement direction in the motorCaminiti, Johnson, & Urbano, 1990), premotor (Burnod et al.,992; Caminiti, Johnson, Galli, Ferraina, & Burnod, 1991), andPC (Battaglia-Mayer et al., 2000, 2005; Lacquaniti, Guigon,ianchi, Ferraina, & Caminiti, 1995). Similar trends of func-

ional properties might exist across the different architectonicreas (Pandya & Seltzer, 1982; Rozzi et al., in press) of the flatxposed part of IPL. A clear gradient has been assessed for someye-related properties across areas 7a and the LIP (lateral intra-arietal area; Barash, Bracewell, Fogassi, Gnadt, & Andersen,991). In the first, neural activity is mainly post-saccadic, in
he second mostly pre-saccadic in nature. Moreover, and moremportant, frontal and parietal areas displaying similar neuronalctivity-types are linked (Fig. 1) by reciprocal association
) between the parietal and the frontal areas involved in reaching. Cortical areasa and Seltzer (1982) for the parietal cortex, by Matelli (see Matelli & Luppino,

cingulated motor areas. Cortico-cortical connections are drawn from Johnsonent areas according to the cytoarchitectonic parcellation of Brodmann. A andemisphere where parts of the parietal and occipital lobes have been removedburied in the medial bank of the intraparietal sulcus and in the rostral bank ofietal sulcus (IPS), “opened” to illustrate the location of the areas buried in the

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onnections (Johnson et al., 1996; Marconi et al., 2001). Thisuggests that in the parietal and frontal cortex eye–hand coordi-ation for reaching emerges as a result of a progressive matchf information, physiologically based on recursive signallinghrough ipsilateral association connections, and refined locallyy intrinsic connectivity, i.e. by short intracortical connections.his interpretation is consistent with a number of experimentalbservations and with the predictions of network modelling.xperimental results (Chafee & Goldman-Rakic, 2000) indi-ate that association connections contribute to confer commonroperties to frontal and parietal neurons. These connectionslay a major role in shaping the network behaviour in relationith both input activation and previous learning, as a Bayesian

ollective decision process (Koechlin, Anton, & Burnod, 1999),here the probability of making a choice changes with the accu-ulation of new information. Furthermore, populations of units

hat combine retinal, hand, eye signals, and linked by recurrentxcitatory and inhibitory connections are necessary to shapehe directional tuning properties of SPL neurons (Mascaro etl., 2003). When lateral inhibition is removed from a recurrentetwork, these tuning properties do not emerge any more.

From a theoretical point of view, in the parieto-frontal inter-lay, each population of parietal cells can combine or match twoistributed signals (for example, arm position and visual targetocation) to compute a third one, such as a motor command.

odeling studies (Deneve, Latham, & Pouget, 2001; Pouget,eneve, & Duhamel, 2002) suggest that the same matchingnit (Burnod et al., 1999) can perform three parallel compu-ations on each pair of inputs signals, in order to compute a
hird one. The same parieto-frontal network can perform differ-nt computations, such as from one set of sensory coordinateso another (inter-sensory predictions), from any sensory to any
otor coordinates (sensory-motor transformations or inverse

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ig. 2. The global tuning field of parietal neurons. Macaque monkeys made arm and/rigin. Significant preferred directions (PDs, colored arrows) of cell activity computeds the mean resultant vector. For SPL neurons: reaching to foveal (red), and to extrafovblue). For IPL neurons: reaching to visual targets (red); reaching to peripheral mexation (green); eye movements to memorized targets (yellow); No-Go (purple). Theask epochs (see below for acronyms). For each cell, PD vectors cluster within a resattaglia-Mayer et al., 2000, 2001). The acronyms IS, M, RT, MT, THT indicate instru

espectively; subscripts e and h stand for eye and hand, respectively. Each acronymattaglia-Mayer et al., 2000, 2001.)

hologia 44 (2006) 2607–2620 2609

odels), and from any motor to any sensory coordinates (for-ard models). Thus, coordinate transformation for eye–hand

oordination during reaching might emerge in the operationsf the parieto-frontal segment of the network, while the fronto-arietal connections, by providing information about the sensoryonsequences of motor plans, might contribute, together witheed-back information, to the composition of forward modelsf movement. Furthermore, such networks with combinatorialroperties and recurrent connections (attractor dynamics) dis-lay a crucial emergent property, i.e. the partially shifting recep-ive fields and tuning of neurons, as experimentally observedn different parietal areas (Duhamel, Bremmer, BenHamed, &raf, 1997; Stricanne, Andersen, & Mazzoni, 1996).If the parietal lobe were subdivided into several mod-

les, each of which associated to a particular frame of refer-nce (gaze-centered, head-centered, hand-centered, etc.), eacheuron should have multimodal tuning properties coherentlyemapped in the frame of reference encoded by that module.y contrast, experimental results show partially shifting recep-

ive fields in areas such as VIP and LIP (Duhamel et al., 1997;tricanne et al., 1996). In different SPL areas, such as PEc,6A, and 7 m, that are only in part coextensive with the so-

alled parietal reach region (PRR; areas MIP, part of PEa, partf V6A; Batista, Buneo, Snyder, & Andersen, 1999), the pre-erred directions of neurons, computed during different epochsf different eye–hand tasks, partially align to each other in aestricted part of space, their global tuning field (GTF; Battaglia-

ayer et al., 2000, 2001; Fig. 2). This indicates a coexistencef different matching operations in the same cortical region.

similar prediction is made by network models with combi-atorial properties (basis functions) and recurrent connectionsDeneve et al., 2001; Pouget et al., 2002). Such networks haveptimal properties of Bayesian statistical inference, and imple-

or eye movements in eight different directions, starting from a common centralduring different epochs of various eye–hand motor tasks. The thick grey arrow

eal targets (green); saccadic eye movements (yellow); delayed reaching in lightmorized targets (blue); reaching to peripheral memorized targets with central

orientation of PDs of typical SPL and IPL neurons is shown across differenttricted part of the workspace, referred to as global tuning field (modified fromction signal, memory delay, reaction time, movement time, target holding time,is color-coded (see above), depending on the behavioral task. (Modified from

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ent a close approximation of a maximum likelihood estimator.urthermore, combinatorial networks display different crucialdvantages relative to those encoding in a single reference-frameAndersen & Buneo, 2002; Batista et al., 1999). The main one ishat their dynamics can weight each synaptic input depending onhe context (for instance the reliability of inputs), and adjust theynaptic weights to confer to the network optimal properties ofayesian statistical inference (Deneve et al., 2001; Pouget et al.,002). These connections shape the profile of activation in theetwork, based on both input activation and previous learningKoechlin et al., 1999).

It is also known that different temporal activity profiles (seeeorgopoulos, Crutcher, & Schwartz, 1989; Johnson et al.,996; Kubota & Hamada, 1979; Tanji & Evarts, 1976; Wienrich

Wise, 1982; Wienrich, Wise, & Mauritz, 1984) coexist ineurons that share the same combinatorial tuning properties. Inoth the parietal and the frontal cortex, neural activity can beime-locked to sensory stimuli, especially when these indicatehe location of the target, to the direction of a future eye–hand

ovement, to motor commands, or be modulated during anntervening delay-time between sensory stimuli and motor out-ut. Delay periods are generally of two types. Memory-delaysrecede movement to targets kept in the buffer of the workingemory, while instructed-delay-times impose a temporal gap

etween target presentation and movement onset, with the tar-et always present in the experimental scenario. It is believedhat neural activity in these epochs selectively anticipates andredicts the upcoming motor output, in relation to arbitrary taskemands, therefore on the basis of expected reinforcement con-ingencies. In this conceptual framework, the input of task selec-ive time-control elements, here referred to as condition unitsBurnod et al., 1999), on the basis of reinforcement contingen-ies, may determine when the prediction made by parietal cellsill be transformed into movement. The properties of condi-

ions units mimic those of cells, mostly represented in the frontalobe, ideally suited to store correlations between sensory-motornd reinforcement signals (for a network model, see Guigon,orizzi, Burnod, & Schultz, 1995).If one accepts this view, a question arises: does the functional

rchitecture of the parieto-fronto-parietal network impose con-traints on the coordinate transformations underlying visually-uided reaching? Our answer is, definitely, yes. Under this view,n fact, reaching cannot be seen as the result of a sequence ofoordinate transformations, each performed by a given corticalrea in its own coordinate frame, or by a number of them in anique coordinate system (Andersen & Buneo, 2002; Batista etl., 1999), but as the outcome of a recursive process where dif-erent signals are selected and combined in a context-dependentashion throughout the network, and further elaborated locally,hanks to intrinsic connections. This interpretation, derived fromhysiological and anatomical studies, is in line with the results oflarge number of behavioral studies stressing the hybrid, task-ependent, and probabilistic nature of the reference-frames for
eaching, as well as the independent coexistence of multiplerames. These studies indicate that the frame of reference usedo specify the endpoint of reaching depends on available sensorynformation, task demands, structure of the visual space, as well
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hologia 44 (2006) 2607–2620

s on the cognitive context (see Battaglia-Mayer et al., 2003 forreview).

Studies of parietal patients show how disturbances of reach-ng, such as optic ataxia, can occur under different reference-rames (Buxbaum & Coslett, 1998; Khan et al., 2005), whileovements disorders of neglect seem to reflect a deficit of

ncoding arm movement direction as an abstract parameterBattaglia-Mayer, Mascaro, Brunamonti, & Caminiti, 2005;usain, Mattingley, Rorden, Kennard, Driver, 2000; Mattingley,radshaw, & Phillips, 1992; Mattingley, Husain, Rorden,ennard, & Driver, 1998).

In conclusion, the constraints imposed by anatomy to physi-logy, the dynamic properties of neurons and their combinatorialperations, the results of psychophysical studies in humans, theask-dependent nature of the movement disorders that followPC lesions, suggest that the nature and demands of the taskelect at any given time the appropriate combination of infor-ation, thus determining the coordinate frame within which this

ccurs. As said before, a different view holds that reaching isncoded by different areas of the PRR (Fig. 3), in a common eye-entered reference-frame (for a review, see Andersen & Buneo,002). This view can hardly be reconciled with the observa-ion that the overwhelming majority of SPL neurons displayGTF (Battaglia-Mayer et al., 2000, 2001), i.e, an invariance

f eye- and hand-related cell’s preferred directions, when stud-ed under different forms of eye–hand coupling, and within a

ultiple-task approach. This invariance rather suggests a cod-ng scheme in allocentric coordinates. It has been previouslyescribed (Andersen & Buneo, 2002; Batista et al., 1999; Calton,ickinson, & Snyder, 2002), that SPL neurons show selec-

ive activation for reaches with respect to saccades. By usingmultiple-tasks approach we have reported that most SPL cellsombine eye and hand related signals (Battaglia-Mayer et al.,000, 2001), although with different strength, depending on therea considered. For these reasons, we believe that the com-inatorial coding scheme for reaching adheres more closely toxperimental evidence, and is theoretically more solid than theommon eye-centered frame discussed above. It is worth notic-ng that the eye-centered scheme has been described for the PRR,hat should include area MIP, parts of V6A and PEa, while theTF has been found in areas V6A, PEc, 7 m and, recently, in

rea 7a as well (Battaglia-Mayer et al., 2005). Until now theRR has not been precisely characterized in terms of location,xtent and cortico-cortical connectivity, as it has been done forhe SPL region where the GTF has been found (Battaglia-Mayert al., 2001; Marconi et al., 2001). Therefore, a direct compari-on of the above discussed coding schemes for reaching in PPCs not yet possible. Furthermore, the PRR is only a limited partf the parietal cortex devoted to reaching (Fig. 3). Therefore, theypothesis that PPC encodes reaching in a unique eye-centeredeference-frame has to be circumscribed to mechanisms occur-ing exclusively within the PRR, and has to be taken with caution,ot only for what was illustrated before, but also considering that
ecent studies of cell activity in a region that is included in theRR has shown that encoding hand movements in the context ofcopy task (Averbeck, Chafee, Crowe, & Georgopoulos, 2005)ccurs in hand rather than in eye coordinates.

A. Battaglia-Mayer et al. / Neuropsychologia 44 (2006) 2607–2620 2611

Fig. 3. The multiplicity of reaching-related regions of the parieto-frontal system. Lateral and medial views of the monkey’s brain showing the cortical areas wherer viewr n of t

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eaching-related activity has been described (red spots; for a comprehensive reegion flanking the intraparietal sulcus. Encircled in blue is the tentative locatio

. Reaching to moving targets: neurophysiologicalechanisms in the primate cerebral cortex

The above mentioned studies are at the core of the analy-is between neural activity and reaching in the cerebral cortex.hey all refer to arm movement toward stationary visual tar-ets. However, both physics and our daily behaviour indicatehat we live and move in a four-dimensional spatio-temporalontinuum. When planning hand movements to visual targets,he specification of spatial parameters, such as initial and finalosition, direction, extent, etc., cannot guarantee a successfulerformance if the visual is not stationary, but in motion. Tontercept a moving object, knowledge of where and when thempact will occur is essential. An influential theory concerningemporal estimations during interception of moving targets isepresented by the τ model (Lee, 1976), according to which annterception movement begins when the ratio between the reti-al size of an approaching object to its rate of change reachescritical (τ) threshold. A more comprehensive formulation of

his theory (Lee, 1998) generalizes the model to guidance ofovements under virtually all conditions, and re-defines τ as

he time-to-closure of the gap existing between the effector andhe target, at the current gap closure rate. The neural underpin-ings of these processes have been extensively studied at thesychophysical level. In the last 20 years, neurophysiologicalxperiments on this issue have been performed mostly on birdsnd insects (Hatsopoulos, Gabbiani, & Laurent, 1995; Judge

Rind, 1997; Lee & Reddish, 1981; Regan & Gray, 2000;ind & Simmons, 1999; Sun & Frost, 1998), and have pro-ided evidence for neural representation of τ, used to drive motoresponses toward moving stimuli. Only recently has the relation-hip between neural activity and time prediction for interception
ovements been explored in the cerebral cortex of primates (seeerchant & Georgopoulos, 2006).These studies have for the most part focused on the role of the
otor and PPC. Motor cortical cells activity was recorded while

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see Battaglia-Mayer et al., 2003). The inset represents an enlargement of thehe so-called parietal reach region (see Andersen & Buneo, 2002).

onkeys were required either to intercept a moving target, oro remain immobile during target motion (Port, Kruse, Lee, &eorgopoulos, 2001). The majority of cells studied were modu-

ated during both the interception and the no-go task, since theyere influenced by signals such as direction of stimulus motion

nd acceleration, and by the time elapsing between the target-nset and its arrival and the interception point, i.e. target-motionime. Two alternative models were tested. The threshold distanceodel (Collewijn, 1972) predicts that interception movements

re initiated when the target reaches a threshold distance afterts presentation, and underlies a reactive strategy. The thresholdmodel implies a predictive strategy, and provided a better fit of

he data. A cluster analysis (Lee, Port, Kruse, & Georgopoulos,001) of motor cortical cells revealed a predominant relation-hip with hand kinematics, while some clusters displayed anearly” activation related to the interception task. Such activityonveyed information about the initial target velocity, a signalecessary for an accurate timing of initiation of the intercep-ion movement. The evolution in time of neural activity in M1onveyed information related to a first-order estimate of time-o-target interception.

In a more recent study (Merchant, Battaglia-Mayer, &eorgopoulos, 2004) neural activity was recorded in parietal

rea 7a and in the motor cortex during interception of targetsoving circularly with real or apparent motion. The results

evealed that a distributed parieto-frontal system underlies thisrimate’s skill. In fact, cells sensitive to the task’s sensory andotor components, i.e., different aspects of stimulus motion

nd hand motor parameters, were found in both the parietal andotor cortex. However, the activity bound to stimulus motion

eatures predominated in area 7a, while that linked to handovement was more commonly observed in the motor cortex

Fig. 4A and B). This aspect is also evident from the temporalrofile of the population activity in the two areas. While parietaleurons show an earlier activation that is best aligned to thetimulus onset, in the motor cortex the onset latencies of neural

2612 A. Battaglia-Mayer et al. / Neuropsychologia 44 (2006) 2607–2620

Fig. 4. Neural mechanisms for interception of moving targets in parietal and frontal cortex. A and B. Population spike density functions of neurons in the motor cortex(filled grey) and in area 7a (open black) with significant modulation during the interception task, at different angular velocities (degrees/s) of stimulus motion. Thegraphs are aligned (0 s) at to the onset of the stimulus motion (A), and to arm movement onset in the interception task (B). In each row, black rectangles represent in(A) the mean ± S.D. of the arm movement onset, and in (B) the mean ± S.D. of the stimulus motion onset. C and D. Population spike density functions of a subset ofn eptiont vemes

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eurons in the motor cortex, that were significantly modulated during the intercask) in eight different directions (D). Neural activity is aligned to the arm motimulus onset. (Modified from Merchant et al., 2004).

ctivity are best aligned to the beginning of movement (Fig. 4And B). A population of cells was task-specific, being activateduring interception of moving targets, and not during movemento stationary target (Fig. 4A–C). Therefore, the distributedystem underlying interception in the primate’s cerebral cortexs not based on a rigid segregation of signals in different corticalreas, but rather on gradients where different neural activityypes relevant to the task are represented at all nodes of theetwork, although with different strength.

Finally, it was found that the psychometric performance inumans and monkeys under conditions of interception of realnd apparent motion is very similar. This prompted a directomparison between the accuracy of performance in humansequested to detect apparent moving stimuli and the predict-ng power of 7a neural activity in estimating the time-varyingosition of a moving target. Decoding of spike-trains showedhat embedded in area 7a’s neural activity is a signal con-erning the target position in real and apparent motion con-itions, a signal important to initiate an interception move-
ent (Merchant et al., 2004). The neural image of the stimulus
osition was very accurate at all speed of real motion, whilen the apparent motion condition only stimulus speeds above00◦/s were reconstructed accurately from neural activity. At

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task (C), but not when the monkey reached to stationary targets (center → outnt onset (0 s). Black rectangles in each row represent the mean ± S.D. of the

his speed, apparent motion is perceived as continuous by humanubjects.

To better understand the neural mechanisms of reaching tooving objects, one can ask how the neural encoding of infor-ation relates to different types of object motion. A recent study

Merchant, Battaglia-Mayer, & Georgopoulos, 2001) has ana-yzed the influence of different moving visual stimuli on theeural activity of various areas of the parieto-frontal network.t was found that optic flow exerts a significant influence notnly, as already known, on PPC, but also on motor cortical cellsctivity. Furthermore, among the different flow fields tested,xpanding flow fields were the most effective in driving neu-al activity in motor cortex. These effects were observed in thebsence of any future movement requirement and, therefore,eflected information available to the motor cortex for poten-ial movements. In parietal area 7a, instead, the modulationxerted by expanding flow fields was the strongest among thoseested. Although in area 7a the percentage of cells sensitive toisual stimuli was three times higher than in motor cortex, in
he latter the sensitivity to expanding flow fields, was twicehat observed in the former. This type of optic flow providesnformation about the direction of an object moving toward anmmobile observer and can also be useful when self-motion and

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bject motion interact, such as when avoiding obstacle or inter-epting visual targets during locomotion. Therefore, the motorystem can access and use the visual information provided byhe moving targets. A potential source of optic flow signals tohe motor cortex is the parietal area PEc (Battaglia-Mayer et al.,001; Raffi, Squatrito, & Maioli, 2002), thanks to its connectionso dorso-caudal premotor cortex (Johnson et al., 1996; Matelli,ovoni, Galletti, Kutz, & Luppino, 1998; Marconi et al., 2001),hich in turn projects to motor cortex. As observed in a previ-us study (Siegel & Read, 1997), parietal cells sensitive to opticow did not display “opponent vector organization” (Motter &ountcastle, 1981; Motter, Steinmetz, Duffy, & Mountcastle,

987; Steinmetz, Motter, Duffy, & Mountcastle, 1987), a fea-ure of parietal visual neurons that can be important in processinghe radial motion of objects moving towards or away from theovea. Thus, encoding object motion in the parietal cortex mighteside on separate parallel mechanisms, segregated in differentopulations of neurons, one based on optic flow information andelated to global motion, another on opponent vector organiza-ion, mostly devoted to local motion analysis.

In all the above studies, recordings were performed in theotor cortex and in the parietal cortex, where they were assigned

o area 7a. This part of the inferior parietal lobule has been subdi-ided in two different areas, Opt and PG, which are reciprocallyonnected through local intracortical fibres (Pandya & Seltzer,982; Rozzi et al., in press). Opt projects to PGm (7 m) in theesial aspect of the parietal cortex (Leichnetz, 2001; PandyaSeltzer, 1982). PGm has reciprocal connection with pari-

tal areas that project to the dorsal premotor cortex, such asE and PEa (Leichnetz, 2001; Pandya & Seltzer, 1982) as wells direct projections to both the rostral and caudal dorsal pre-otor cortex (Johnson et al., 1996; Matelli et al., 1998; Marconi

t al., 2001), while PG is connected to the dorso-caudal pre-otor cortex, although this connection does not seem to be a

ubstantial one. Therefore, these connections can be a substratef the parieto-frontal interplay necessary for reaching to movingargets, a process where recurrent signaling can provide a con-inuously refreshed neural image of target position over time,o be used and incorporated into the upcoming motor commandecessary for interception.

An interesting type of interception consists of catching freealling objects (Lacquaniti & Maioli, 1989). Studies in humansave revealed that during this task the brain uses an internalodel of gravity, that accounts not only for the object’s veloc-

ty, but also for its acceleration (McIntyre, Zago, Berthoz, &acquaniti, 2001; Zago et al., 2004), a parameter otherwiseoorly estimated by the visual system (for a discussion, seendovina et al., 2005). This process is context dependent, sincenterception of a moving target on a video monitor occurs assum-ng a non-accelerated motion, even when the motion is accel-rated. A recent fMRI study (Indovina et al., 2005) suggestshat the gravitational acceleration in visual motion is encodedithin a distributed network centred on the so-called “vestibular

ortex”, a region of the parieto-temporal cortex that in humansas been described on the basis of different methods. This regionight be the homologue the so-called “parieto-insular vestibular

ortex” of monkeys (for a review, see Guldin & Grusser, 1998).

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hologia 44 (2006) 2607–2620 2613

ow the information about gravitational motion encoded in thevestibular” cortex becomes available to motor cortex remainso be determined, although the cortical pathway whereby theirnterplay might occur seems to include the premotor cortex thats also significantly activated in the study by Indovina et al.2005).

. Neural mechanisms of correction of hand movementrajectory

The ability to correct on-going movements is a commonxperience of everyday life. Psychophysical studies have shownhat the reaction time needed to correct an ongoing movementn the case of a large target displacement is around 100 msCarlton, 1981; Georgopoulos, Kalaska, Caminiti, & Massey,983). Given enough time for correction, the hand will not reachhe first target, but produce a curved trajectory toward the sec-nd one. Moreover, rapid hand reaches can also be correctedven when the subject is not consciously aware of the shift inarget position, as when the target is moved during an ocularaccade (Blouin, Teasdale, Bard, & Fleury, 1995; Desmurgett al., 1999; Pelisson, Prablanc, Goodale, & Jeannerod, 1986).utomatic corrections in response to a modification in target

ocation also occur when vision of the arm is occluded (Pelissont al., 1986), and in deafferented patients with loss of propri-ception in all four limbs (Blouin et al., 1995). These resultsuggest that the nervous system continuously monitors ongo-ng movements, and modify them at any time, if requested by aime-varying scenario (Georgopoulos et al., 1983; van Sonderen,ielen, & Denier van der Gon, 1989). It has been hypothesized

hat the ability to perform quick online corrections resides ineedback mechanisms based on motor outflow, or on internalepresentations of movement, as well as on sensory informa-ion, principally visual signals such as retinal error (Blouin etl., 1995; Desmurget et al., 1999).

Only one neurophysiological study has addressed the ques-ion of the neural basis of online movement corrections. In therimary motor cortex (Georgopoulos et al., 1983), the patternf neuronal activity related to hand movement to a first target isruncated upon presentation of a second one, and is replaced bypattern of activity similar to that observed during movement

rom the starting point to this new target. The origin of this sig-al is not known, although several lines of evidence support arucial role of the PPC in the online movement corrections. Pri-ate studies (for a review see Battaglia-Mayer et al., 2003) have

hown that parietal neurons display activity related to eye andand movements, to the spatial position and direction of motionf a visual stimulus, as well as to its attentional load. Directvidence was obtained in humans, where perturbation of PPCctivity by transcranial magnetic stimulation disrupts the abilityo correct hand movement in response to a change in target loca-ion (Desmurget et al., 1999). In this context, it is worth noticinghat transient disruption of PPC function through TMS occur-
ing before the onset of a saccade does not alter the saccades,ut disrupts the natural coupling existing between the ampli-ude of saccades and reaches (Van Donkelaar, Ji-Hang, & Drew,000). Finally, a case report (Pisella et al., 2000) has shown that

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patient with optic ataxia from bilateral PPC lesion was unableo produce smooth corrections of hand trajectory following aapid change of target location. Instead, the hand moved to therst and then to the second target.

Ongoing studies of the parietal cortex in our labArchambault, Battaglia-Mayer, & Caminiti 2005) haveddressed this problem in alert monkeys trained to make regu-ar reaches, as well as fast corrections of reach trajectories aftersudden jump of the visual target in three-dimensional space.imilar tasks were also performed in a saccadic paradigm, in

he absence of hand movement. The detailed kinematics of handnd eye movements showed that after a target jump, while theye moved to the first and then to the second target, the handmoothly changed its initial trajectory to the first target to moveoward the second one (see also Georgopoulos et al., 1983).here were no difference in the early phase of movement tra-

ectory in the perturbed versus the non-perturbed trials. In spitef this, after target jump, an early change of neural activity waseen in a good proportion of cells. Such predictive signals con-erning the future correction of movement trajectory were alsovident in another population of parietal neurons that encodedand tangential velocity (see also Averbeck et al., 2005). Theseells modulated their firing frequency in a way that preceded byvariable time (mean: 90 ms) the abrupt change in hand velocityccurring shortly before the change of trajectory (Fig. 5). Somef these cells, as well as other parietal neurons studied in theame region, also fired after the change of movement direction,uggesting that in PPC predictive signals coexist with feed-backnformation concerning ongoing movement. Thus, these popu-ations of neurons could be a substrate for the neural mechanismhereby the parietal cortex can control and promote modifica-

ions of hand trajectory at all times during movement, dependingn the incoming sensory signals.

These predictive signals can be addressed to the motor cortex,ia ispilateral cortico-cortical connections that link the SPL tohe dorsal premotor areas (Johnson et al., 1996; Matelli et al.,998; Marconi et al., 2001).

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ig. 5. Activity of a parietal neuron during hand movement without (single-step) anell is displayed for hand reaching movements starting from the centre of the cube tourves) and the hand velocity signal (shaded grey curves) are aligned to the beginninarget presentation and the thick horizontal lines correspond to periods of eye movemas well correlated with hand velocity, leading it by an average of 65 ms. (B) Data fr

hen was extinguished at the initiation of movement time and target 8 was lit (1–8),receding the two peaks in the hand velocity profile. Hand paths for the 8–1 task arellustrated).

hologia 44 (2006) 2607–2620

. Understanding the motor disorders of parietalatients from a neurophysiological perspective

It is our hypothesis that the functional architecture of thearieto-frontal system in general, and the dynamic operationserformed by PPC in particular, can provide a positive image ofhe motor disorders that in humans are a dramatic consequencef damage to the PPC. The hallmarks of motor disorders of thearietal syndrome are optic ataxia (OA) and directional hypoki-esia (DH). Both includes a constellation of different clinicaligns.

.1. Main features of optic ataxia and directionalypokinesia

Patients with OA (for a recent review, see Battaglia-MayerCaminiti, 2002; Rossetti, Pisella, & Vighetto, 2003) fail to

roperly reach or grasp objects under visual control, and showsevere alteration of the spatial and temporal characteristics oforrective movements prompted by changes in target location.n-flight corrections of the direction of hand movement occurate in time and are not characterized by the smooth curvaturef hand trajectory toward the second target’s location, typicalf normal subjects. In these patients, the hand completes theovement toward the first target, and then moves toward the sec-

nd one (Grea et al., 2002). Obstacles avoidance during reachess impaired (Schindler et al., 2004) in these parietal patients.A is a task-dependent disorder, since it occurs for reaching orrasping for real targets, not when pantomiming hand graspingovement of memorized objects (Milner et al., 2001). OA can be

onsequence of bilateral or unilateral PPC lesions (see Milner,aulignam, Dijkerman, Michel, & Jeannerod, 1999; Perenin &ighetto, 1988; Pisella et al., 2000; Rossetti et al., 2003). In all

nstances, reaching errors mostly occurs in the peripheral visualeld (see Rossetti et al., 2003 for a discussion). After unilatateral

esions, the features of the resulting deficit will depend on theemisphere that is affected. Lesions confined to the right PPC,

d with (double-step) change in target location. (A) The activity of one parietaleach of the 8 peripheral targets (numbers). Both the neural activity (thick blackg of hand movement (vertical dashed line). The triangles indicate the time ofents. Neural activity was modulated with the direction of hand movement andom the same cell is shown for the condition where target 1 was presented first,or vice-versa (8–1). Note the presence of a double peak in the cell’s activity,depicted inside the cube. This cell was not active in the eye control task (not

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esult in misreaching with one or both hands in the contralateralisual field (field effect). After left parietal lesions, misreachings observed with the right hand in both ipsi- and contralateralisual fields (hand effect). When left lesions severely affect thePL (Perenin & Vighetto, 1988), or when a on-line change ofovement trajectory is required (Grea et al., 2002), OA is not

nly confined to the peripheral visual field, but occurs in centralision as well.

Directional hypokinesia (DH) in neglect patients consists inn elongation of hand reaction and movement time for targetn the contralesional space (Heilman, Bowers, Coslett, Whelan,

Watson, 1985; Husain et al., 2000; Mattingley et al., 1992,998). The disorder affects the ispilesional arm as well, andherefore is different from “motor neglect”, that consists in aeneral reluctance to move the contralesional arm. DH oftenoexists with directional bradykinesia and hypometria, so thatrm movements have reduced velocity and amplitude as well. Inhese patients, similar disorders are common in the oculomotoromain (Girotti, Casazza, Musicco, & Avanzini, 1983; Niemeier

Karnath, 2003; Pierrot-Deseilligny, Rivaud, Gaymard, Agid,991; for review see Husain & Rorden, 2003). In fact, sac-ades to contralesional visual targets are delayed, hypometricnd their trajectories show a “staircase” shape (Girotti et al.,983). Although DH has been the basis of directional motorodels of neglect (Heilman et al., 1985), today it is widely

ccepted that it cannot explain the entire constellation of symp-oms of neglect patients (Husain & Rorden, 2003). Therefore,e will consider DH per se, independently of the other disorders

hat characterize neglect.

.2. Parietal lesions leading to optic ataxia and directionalypokinesia

The lesion responsible for OA has traditionally been consid-red as centred on the intarparietal sulcus, mainly involving thePL at the parieto-occipital junction (Vallar & Perani, 1986;erenin & Vighetto, 1988; for recent reviews see Battaglia-ayer & Caminiti, 2002; Rossetti et al., 2003). A qualita-

ive study (Nagaratnam, Grice, & Kalouche, 1998) of five OAatients has shown that three of them had posterior parietalesions, while the remaining two suffered from frontal damage.ase reports are available of “crossed OA” involving the corpusallosum (Ferro, Bravo-Marques, Castro-Caldas, & Antunes,983), and of OA of “subcortical” origin (Classen et al., 1995).recent study (Karnath & Perenin, 2005) has moved the locus

f OA from SPL to the IPL. A critical analysis of the anatomy ofesions in these parietal patients reveals significant involvementot only of IPL, but also of SPL, as well as a massive involve-ent of fibres tracts of the white matter. In addition, the lesion

ften extended to the precuneus, i.e., the mesial part of the upperector of parietal cortex that anatomically has to be ascribed toPL. Therefore, the conclusion that IPL is more involved thanPL is rather surprising, also considering that in such a study

he origin and destination of the fibres tract affected was notetermined.

DH has generally been considered a sign of output-related,r “premotor” components of neglect (Heilman, Valenstein, &

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hologia 44 (2006) 2607–2620 2615

atson, 2000; Watson, Miller, & Heilman, 1978; for reviewsee Fink & Marshall, 2005; Vallar, Bottini, & Paulesu, 2003).tudies of neglect patients with inferior frontal and IPL lesionsave shown hand movement disorders of directional nature onlyn parietal and not in frontal patients (Husain et al., 2000;

attingley et al., 1992, 1998), thus attributing a cognitive-motorole to the IPL. Although recent studies have assigned a cru-ial role in neglect to lesions of the superior temporal cortexather than of the IPL (Karnath, Ferber, & Himmelbach, 2001;arnath, Fruhmann Berger, Kuker, & Rorden, 2004a; Karnath,ruhmann Berger, Zopf, & Kuker, 2004b), Hillis et al. (2005)ave reported that egocentric neglect is mostly associated withypoperfusion of the right angular gyrus (Brodman’s area 39)n IPL, while allocentric neglect to hypoperfusion of the rightuperior temporal gyrus (Brodman’s area 22).

It is worth stressing that in most parietal patients, the lesionenerally encroaches the intraparietal sulcus, involving bothPL and IPL at varying degrees. Therefore, it is reasonable

o assume that some features described as typical of OA, suchs its occurrence mainly in the contralateral visual field, mighte due to the influence of a direction specific disorder, suchs DH. In fact, when the parietal lesion mainly involves thePL, misreaching with the contralesional hand can be seen notnly in the contralateral, but also in the central and ipsilateralisual fields (Perenin & Vighetto, 1988). Therefore patients withA from parietal lesions involving both SPL and IPL shouldlso be tested specifically for DH, not merely for hemispatialeglect.

.3. Optic ataxia, directional hypokinesia, and the visualontrol of reaching

If the anatomical damage responsible for OA was IPL andot SPL, the visual control of arm movement would criticallyepend on the former, not on the latter. This conclusion haseen drawn by Karnath and Perenin (2005), also on the basis ofcritical analysis of lesion studies in monkeys. When comparinguman with monkey studies, it must be stressed that in monkeys’euroanatomical (Pandya & Seltzer, 1982) and neurophysiolog-cal literature SPL includes areas PE, PEa, MIP, PEc, PGm, and6A (Fig. 1). Reaching-related activity has been described in all

reas of this distributed system (Fig. 3; for a review see Battaglia-ayer et al., 2003). Furthermore, in monkeys the main source

f visual input to dorsal premotor and motor cortices is SPLJohnson et al., 1996; Matelli et al., 1998; Marconi et al., 2001;or a review see Caminiti, Ferraina, & Johnson, 1996), sincehere are no major projections from IPL to the dorsal premotorreas that project to motor cortex.

The contribution offered to the issue of visual control ofovement by lesion studies in monkeys unfortunately lacks

onsistency. Most of these studies were performed before theurrently accepted parcellations of PPC were described. Fromhe late fifties to about the end of the seventies an extensive lit-
rature (see Hartje & Ettlinger, 1974; Lamotte & Acuna, 1978)howed defects of visual guidance of reaching after PPC lesionshat unfortunately extended over both SPL and IPL. This litera-ure will not be dealt with in this context. When lesions studies

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Rushworth, Nixon, & Passingham, 1997) were guided by moreefined architectonic and functional subdivisions of PCC, mis-eaching in the light was observed after bilateral removal of IPLreas 7a, 7ab and LIP, while reaching inaccuracy in the darkas observed after bilateral lesions of SPL areas 5 and MIP,

nd of IPL area 7b. However, in the last case, the most severempairment in visual control of arm movement were seen in thenimal were the lesion extended into the mesial aspect of SPLffecting area PGm (7 m) as well. This is not surprising if oneonsiders that neural activity in area 7 m is deeply influenced byisual feed-back signals about hand movement trajectory andand position (Ferraina et al., 1997a,b). Rushworth et al. (1997)tress that their SPL lesions “did not remove all of the visuallyesponsive areas in the depth of posterior medial bank of thePS. . .”. In a more recent analysis (Battaglini et al., 2002), bothrasping and reaching movements, although qualitatively mon-tored, were impaired after lesion of area V6a. More important,he distributed nature of the system underlying visual control ofrm movement in primates predicts that only very large lesionsnterrupting the flow of information from the many “parietaleach regions” of SPL (Fig. 1; Fig. 3) to dorsal premotor cortexill severely affect the visual control of movement. This is veryifficult to achieve in a well controlled experiment, and was notttempted in the study by Rushworth and his colleagues. Finally,ost neurophysiological and anatomical studies of motor, pre-otor, and parietal cortices of monkey indicates that all informa-

ion necessary for the composition, execution and visual controlf reaching are encoded and combined in the SPL (for recenteviews see Andersen & Buneo, 2002; Battaglia-Mayer et al.,003). Thus, as far as the cortical control of visual reaching isoncerned, also considering possible differences in parietal cor-ex functions between monkeys and humans, the conclusion ofhe study by Karnath and Perenin (2005) has to be taken withaution.

In humans, DH reveals a disorder of directional nature in theontrol of movement. This can be regarded as a disruption of theundamental mechanisms responsible for the representation ofotor space under visual control. In monkeys, IPL lesions dis-

upt or deteriorate planning and execution of reaches to visualargets in the contralesional space (Deuel & Regan, 1985; Deuel

Farrar, 1993; Ettlinger & Kalsbeck, 1962; Faugier-Grimaud,renois, & Stein, 1978; Faugier-Grimaud, Frenois, & Peronnet,985). Reaction and movement times are generally elongatedsee however Faugier-Grimaud et al., 1985) and reaching move-ents are inaccurate even when performed with the ispilesional

rm (Deuel & Regan, 1985; Faugier-Grimaud et al., 1985). Thisast observation is of some relevance since it allows a distinc-ion between motor neglect and DH not only in humans, but in

onkeys as well.

.4. A positive image of optic ataxia and directionalypokenesia

Neurophysiological and neuroanatomical studies in monkeysuggest that OA can be interpreted (Battaglia-Mayer & Caminiti,002) as the result of the breakdown of the combinatorial mech-nisms occurring within the GTF of parietal neurons, where

dott

hologia 44 (2006) 2607–2620

etinal, eye, and hand related signals are combined on the basisf task contingencies.

This is a general interpretation that, of course, neither cap-ures the hemispheric difference in the consequences of lesions,or explains all the specific signs and subtypes (see for instanceackson, Newport, Mort, & Husain, 2005) of OA. In spite ofhis, the dynamic properties of SPL neurons and their role inhe parieto-frontal system predict different forms of inaccuracyf reaching. For instance, SPL lesions in the left hemisphereesult in misreaching occurring throughout the entire work-pace, as predicted by the uniform distribution of the meanectors of the GTF of SPL neurons. Furthermore, within theTF, the spatial relations between different preferred direc-

ions express not only coupling, but also decoupling of eyend hand movement and position. SPL neurons can distinguish,hrough differences in orientation and depth of their tuningunctions, conditions when the eye and the hand coincide fromhose when they do not. The “angular coding” inherent to theTF might not only be sufficient, but also necessary for those,

till coordinated, eye–hand actions required to maintain the eyend the hand at different places, or to move one relative tohe other, i.e., in decoupled situations. SPL neurons can sub-erve this task, through a mechanisms that computes the angularifference between the orientation of the mean vector of theTF and any given eye and/or hand preferred direction lyingithin it.These observations might provide a basis for interpreting the

eaching errors that occur in peripheral vision, i.e., when eye andand position differ. These relationships are interesting sincehey suggest that the comparison between monkey’s studies anduman’s neuropathology can help the interpretation of neuro-ogical processes in humans based on animal models, as well aso read them out in an evolutionistic perspective.

The failure of OA patients to make fast, in-flight corrections ofand movement trajectory may be due to the loss of those popu-ations of parietal cells whose activity carries a predictive signaloncerning corrections of hand movement direction, promptedy a change of target location.

In the parieto-frontal network, the gradient-like arrangementf these signals is essential for a progressive combination ofnformation (Burnod et al., 1992, 1999) leading to the compo-ition of motor commands for reaching. The collapse of thisetwork and the failure of re-entry might prevent the match ofnformation that shape the collective properties of the parieto-rontal units of the network. In this respect, it is interesting thatstudy of the reaching errors made by OA patients suggests

hat their impairment originates from the visuomotor transfor-ation occurring beyond the parietal cortex, that necessary to

hange into arm-centred coordinates an eye-centred representa-ion of target location (Khan et al., 2005). If so, this observationtrengthens our hypothesis of OA as a breakdown of the inter-lay between parietal and frontal areas and, therefore, as aortico-cortical disconnection syndrome. As far as the context-
ependency of OA is concerned, this can only be consequencef the conditional nature of parietal cell activity, thanks to whichhe combination of the different sources of information seemso be dictated by a task-dependent selection processes.

A. Battaglia-Mayer et al. / Neuropsychologia 44 (2006) 2607–2620 2617

Fig. 6. The representation of the eye and hand directional motor space in area 7a. Distributions of cells’ preferred directions in area 7a, computed during eyereaction-time (a), eye movement-time (b), hand reaction-time (c), hand movement-time (d), across different tasks during which the eye and/or the hand moved tov ovedl is sigB

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isual targets. The same results were obtained when the eye and/or the hand mobule. In all instances (a–d), the distribution of the cells’ preferred directionsattaglia-Mayer et al., 2005).

In a recent study (Battaglia-Mayer et al., 2005), we haveecorded the activity of single cells in area 7a of the IPL whileonkeys performed several eye–hand directional motor tasks,

equiring different forms of eye–hand coordination. The resultsevealed that in area 7a there exists a representation of eye andand motor space that, contrary to that of the SPL, premotornd motor cortex, is highly skewed toward the contralateralorkspace (Fig. 6). The loss of a visuomotor representation thatagnifies the contralateral directional continuum (Battaglia-ayer et al., 2005) or contralateral location of reach targetsight explain the difficulties in the composition of motor com-ands and in the execution of eye and hand movements observed

n neglect patients.The data and hypotheses discussed above conform to theo-

etical requirements (Mesulam, 1999) and to the predictions ofetwork models of neglect (Pouget & Sejnowski, 1997; Pouget

Driver, 2000) that heavily rely on the anisotropy of spatialepresentations. Lesions in one hemisphere will result in lackf information concerning the contralesional visual and motorpace. Thus, the neurophysiological results and interpretationsffered above might provide the neurophysiological underpin-ings and new bases to theoretical models of neglect.

In conclusion, 25 years of study of the parieto-frontaletwork, namely of the dynamic properties of neurons inifferent areas and of their relationships with the pattern ofortico-cortical connectivity in monkeys, offer a picture of theole of PPC that has evolved from the original one, that of aontrol exerted by its different sectors on eye (IPL) or handSPL) visuomotor behaviour, into the current one (Battaglia-

ayer et al., 2000, 2001, 2005; Ferraina et al., 1997a,b, 2001),ased on encoding coordinated eye and hand movement in bothPL and IPL. As such, the current knowledge on PPC functionsrovides new challenges to neuropsychological studies on theonsequences of parietal lesions, together with more solidnd promising bases than hitherto for an interpretation of theovement disorders of parietal patients from a physiological

erspective.

cknowledgments

This study was supported by funds from the Ministry of theniversity and Technological and Scientific Research (MIUR)

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to memorized target locations. Cells were recorded in the left inferior parietalnificantly skewed toward the contralateral right part of space. (Modified from

f Italy. Philippe S. Archambault was supported by the Canadiannstitutes of Health Research and by the MIUR of Italy.

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