T

Ta

b

c

d

e

f

g

a

ARRAA

KAIMSS

hfisdBdirsrisr“sii

j((

0d

Neuropsychologia 48 (2010) 3121–3127

Contents lists available at ScienceDirect

Neuropsychologia

journa l homepage: www.e lsev ier .com/ locate /neuropsychologia

he perception of real and illusory motion in schizophrenia

.J. Crawforda,∗, J.P. Hammb, M. Keanc, A. Schmechtigd, V. Kumarid, A.P. Anilkumare, U. Ettinger f,g

Mental Health and Neural Systems, Department of Psychology, Lancaster University, Lancaster LA1 4YF, United KingdomResearch Centre for Cognitive Neuroscience, Department of Psychology, Auckland, Auckland 92019, New ZealandManchester Medical School, Oxford Road, Manchester, Greater Manchester M13 9PT, United KingdomInstitute of Psychiatry, London, King’s College London, DeCrespigny Park, Greater London SE5 8AF, United KingdomMaudsley Outpatient Department, Maudsley Hospital, Denmark Hill, London SE5 8AZ, United KingdomDepartment of Psychiatry, Ludwig-Maximilians-Universität, Nussbaumstr. 7, 80336 Munich, GermanyDepartment of Psychology, Ludwig-Maximilians-Universität, Leopoldstr. 13, 80802 Munich, Germany

r t i c l e i n f o

rticle history:eceived 18 August 2009eceived in revised form 21 May 2010ccepted 18 June 2010

a b s t r a c t

An illusion of rapid movement is normally perceived when an attentional cue (such as a peripheralflash) preceeds the onset of a line. The movement is perceived as receding away from the cue. Thisstudy investigated how this illusion was perceived by people with schizophrenia. Nineteen participantswith schizophrenia and 26 healthy matched controls were presented with a series of real, illusory, no

vailable online 25 June 2010

eywords:ttention

llusionotion

motion or combined real and illusory motion stimuli at various target speeds. Detection thresholds weremeasured to determine the reliability of motion perception. The participants with schizophrenia were notdistinguished from the control group in the perception of real motion. However, the motion detectioncurves for the schizophrenia group revealed a reduction in the perceptual effect of illusory motion incomparison to controls. The findings revealed that people with schizophrenia may be less easily deceived

paris

chizophreniamooth pursuit eye movement

by illusory motion in com

The environment presents a complex array of signals to theuman sense organs, although we actively respond to only a small

raction of these inputs. A selection of the most relevant signalss necessary to reduce the computational load on the cognitiveystems and to guide action towards a goal. In the early clinicalescriptions of people with schizophrenia Kraepelin (1919) andleuler (1950) documented a severe difficulty in the ability toirect attention. Kraepelin described patients’ difficulties in direct-

ng their attention onto information that was relevant, and in theelease of attention away from irrelevant details. With typical fore-ight, Kraepelin (1919, p. 6) preempted much of contemporaryesearch in proposing that the poor eye tracking of a moving targetn schizophrenia (Diefendorf & Dodge, 1908) might also be due touch difficulties in the control of attention. Bleuler (1950, p. 68) alsoecognized a significant disturbance of attention in these patients;

The selectivity which normal attention ordinarily exercises among theensory impression can be reduced to zero so that almost everythings recorded that reaches the senses. Thus the facilitating as well as thenhibiting properties of attention are equally disturbed”.

∗ Corresponding author.E-mail addresses: t.crawford@lancaster.ac.uk (T.J. Crawford),

.hamm@auckland.ac.nz (J.P. Hamm), Matthew.Kean@manchester.ac.ukM. Kean), Veena.Kumari@iop.kcl.ac.uk (V. Kumari), Anil.Kumar@slam.nhs.ukA.P. Anilkumar), Ulrich.Ettinger@med.uni-muenchen.de (U. Ettinger).

028-3932/$ – see front matter © 2010 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2010.06.027

on to healthy participants.© 2010 Elsevier Ltd. All rights reserved.

People with schizophrenia report changes in the appearance ofvisual objects, a general heightening of perceptual intensity acrossmodalities, objects appear unbearably brighter than they shouldbe; colours are more intense, and background noises are intoler-ably loud. Clinical observations refer to a ‘heightening of sensoryvividness which is experienced particularly in the auditory andvisual fields’ (McGhie & Chapmann, 1961). This would imply anintense and wider diameter beam of visual attention that is diffi-cult to control in terms of the Posnerian Theory of Visual Attention(1980).

People with schizophrenia are generally reported to performpoorly on a number of attentional tasks. It would therefore beof considerable importance to show that there are circumstances,when changes in usual properties of visual attention can enhance,rather than impede, perceptual performance. We reasoned thatthe functional differences in attention might render people withschizophrenia more resistant to visual illusions that are triggered byattentional cues. Some evidence for improved perceptual functionin schizophrenia has already emerged. People with schizophreniawere reported to be less vulnerable to a contrast–contrast percep-tual illusion, where a pattern was presented either in isolation or

together with a surrounding high contrast pattern (Dakin, Carlin,& Hemsley, 2005). Clearly, schizophrenic patients are not as easilydeceived by some visual illusions.

The accurate detection of the speed and direction of a movingobject is a biologically old function that continues to be essential

3122 T.J. Crawford et al. / Neuropsychologia 48 (2010) 3121–3127

F ollowt

ffiebatcNiitymmtstectef

atnmarnPHtpriahswut

ig. 1. Visual depiction of the display and depicting slow real motion to the right fhe left.

or survival. Yet a number of visual illusions indicate that we oftenail to distinguish between real and illusory motion. This reflects,n part, the characteristic neural response to illusory motion. Forxample, illusory line motion (ILM) occurs when one end of a staticar is presented in the vicinity of a recent attentional cue, such asflashing box (see Fig. 1). In this situation the entire bar appears

o be drawn in motion away from the location of the attentionalue (Hikosaka, Miyauchi, & Shimojo, 1991, 1993a). Jancke, Chavane,aarman, and Girinvald (2004) showed that cat visual neurones

n area 18 responded to ILM with a wave of activation that wasdentical to a stimulus that was in real motion, with a velocityhat matched the perceived illusion. The strong neural basis of ILMields some powerful implications for behaviour. For example, inan this illusion can be used to reverse the usual rules of sensori-otor control. Crawford, Kean, Klein, and Hamm (2006) revealed

hat the illusion of rapid motion away from a cue modified thepeed of a saccadic eye movement that is normally triggered rapidlyowards a cue with a sudden onset; so that with the illusion theye movement was now triggered more rapidly away from theue rather than towards it. Recently, Ilg and Their (2008) reportedhat smooth pursuit-related responses from a number of frontalye field neurons to an imaginary target could not be distinguishedrom activity to a real target in motion.

It is not known whether people with a psychotic illness, suchs schizophrenia, perceive illusory line motion in a similar fashiono healthy participants. The idea that patients with schizophre-ia might respond differentially to real and attention-cued illusoryotion emerged from the consideration of the deficits of visual

ttention in this population and the growing recognition of theole of attention on both high and low level perceptual mecha-isms (e.g. Carrasco, Penpeci-Talgar & Eckstein, 2000; Reynolds,asternak & Desimone, 2000). Previous work (Crawford et al., 2006;amm & Klein, 2002) demonstrated a robust illusion of motion in

he ILM paradigm. However, it remained to be determined howeople with schizophrenia would respond to such a stimulus. Weeasoned that there should be distinct effects in the perception ofllusory line motion, given the well-known deficiencies of visualttention in people with schizophrenia. More specifically, whilst

ealthy participants should be subject to the illusion, people withchizophrenia should be less easily deceived by the illusion. In otherords, patients should show superior judgment of veridical motionnder selective conditions, when illusory line motion is in compe-ition with real motion.

ing a right attention cue that is thought to induce apposing illusory line motion to

We used a quantitative measure of the motion percept in orderto contrast real and illusory motion. The illusion can be reducedor cancelled with an inverse real motion stimulus (Steinman,Steinman, & Lehmkuhle, 1995) or other forms of illusory motioninduced by luminance gradients (vonGrunau, Dube, & Kwas, 1996;vonGrunau, Racette, & Kwas, 1996). With a simple two-alternativeforced-choice paradigm of motion direction the cancellation proce-dure can be used to determine the threshold at which the detectionof motion is no longer reliable. We used brief motion targets (belowthe onset latency of smooth pursuit eye movements) to avoid theconfounding effects of smooth pursuit (Hong et al., 2009).

1. Methods

1.1. Participants

Data were collected from 21 participants with schizophrenia and 28 healthycontrol participants. Four participants (two from each group) failed to meet per-formance criteria outlined below, and data from an additional participant from thepatient group was unusable due to a technical failure during the recording of theresponses. The remaining analysis and discussion was based upon the data col-lected from 19 patients (15 males, 4 females: mean age 39.3 years, range = 24–48;education 13.53 range 10–20 years, all right handed) and 26 control participants(17 males, 9 females: mean age 35.3 years, range = 21–56, mean years of education16.37 range 10–23 years; all right handed). The two groups did not differ signifi-cantly in gender (�2 = 0.982 ns), age (t(43) = 1.49 ns), parental social economic status(t(40) = 0.85 ns) and handedness but as expected the patients had lower levels ofeducation (t(43) = 2.84, p < 0.05).

Schizophrenic participants were outpatients in the South London and MaudsleyNHS Trust and were referred by their treating clinicians. Patients had a DSM-IVdiagnosis of schizophrenia (SCID). All patients were treated pharmacologically.Five patients were treated with antipsychotics only, while the remainder wereon antipsychotics and co-medicated with a variety of selective serotonin reuptakeinhibitors, benzodiazepine, or antimuscarinic compounds. The average age at firstcontact with psychiatric services was 22.44 years (SD = 6.99) and the number ofprevious hospitalisations was mean = 3.27 (SD = 1.64). The severity of the patients’clinical symptoms was rated on the day of ILM task assessment using the Schedulefor the Assessment of Positive Symptoms (SAPS; Andreasen, 1983) and the Schedulefor the Assessment of Negative Symptoms (SANS; Andreasen, 1984) with high intra-and inter-rater reliabilities (intra-class correlation coefficients ranged from 0.91 to0.93). The average SAPS score was 7.35 (SD = 2.34) and the average SANS score was9.77 (SD = 3.42).

Controls were recruited using advertisements placed around the local area andemail circulars within the university. All controls were free of a history of psychiatric

disorders as established using the Structured Clinical Interview for DSM Diagnoses(First, Spitzer, Gibbon, & Williams, 1997) and of a history of psychosis in first-degreerelatives. Exclusion criteria for both groups were any neurological illness, headinjury resulting in unconsciousness of more than 5 min, current consumption ofany medication (other than compounds prescribed by the treating clinicians in thepatient group), and any visual impairment (other than the use of corrective lenses).

sycho

TPp

1

(a1smsmdr

s6Tatdpi

1

htmaat

a5rwmtsic

wTaplmgpmTsocdssaamatraiiocb

rtmIt

motion trials during the no flash condition. This revealed no signifi-cant difference (t(43) = 0.38, p > 0.05; mean difference 1.75 and 1.78,for controls and patients, respectively). Thus there was no groupdifference in the perception of real motion, therefore, any group

1 In the absence of this equivalence in the perception of real motion the interpre-

T.J. Crawford et al. / Neurop

his study was approved by the South London and Maudsley and the Institute ofsychiatry Research Ethics Committee. All participants gave their informed consentrior to their inclusion in the study.

.2. Materials

Stimuli were presented on a Gateway 650 computer, comprising of a midi towerATX 200 watt tower case) with a 20-GB 7200RPM hard drive. The computer wasPentium 3 P600 processor, contained an ATI RAGE 128 16 MB graphics card, had28 MB RAM and was designed to run MS DOS. The screen that was used to displaytimuli was a 17-in. Gateway EV700 LG monitor, running at 60 Hz. Responses wereade, through a two-alternative forced-choice task, on a keypad with two side-by-

ide buttons, representing left and right motions, respectively. All responses wereade with the right hand. The millisecond timing routines implemented are those

escribed in Hamm (Hamm, 2001). Display synchronization with the monitor’sefresh cycle was achieved as described by Heathcote (1988).

The diagrammatic representation of stimulus displays is shown in Fig. 1. Alltimuli were monochromatic, on a greyscale of 64 levels with 0 being black and3 white. The fixation point was a small black cross in the middle of the screen.wo light grey (greyscale = 60) square markers (2.5◦ × 2.0◦ per side) were displayedbove the cross, with their centres subtending 0.5◦ to either side of the cross. Thearget line was also light grey (greyscale = 60), 9.5◦ in length and 1.5◦ in height, andisplayed with its ends connecting to each of the two markers. All stimuli wereresented against a neutral grey (greyscale = 50) background. The cue was a sudden

ncrease in luminance (greyscale = 63) of either square markers.

.3. Procedure

The experiment was conducted in a dimly lit room with each subject positioningis or her head on a chinrest 57 cm in front of the monitor. Subjects were instructedo fixate the cross and after stimulus presentation to indicate the direction of the

otion of the target line. When no motion was detected, subjects were asked to trynd distribute guess responses equally on the two response keys and not to choosedefault guess response. These instructions were presented both verbally and on

he computer screen before the commencement of the experiment.A trial began with the presentation of the fixation cross, the two square markers,

nd the bar joining the two markers. This display was presented for a duration of00 ms. On cue trials either the left or right marker increased its luminance and theneturned to its starting luminance after 50 ms. Upon cue offset the connecting baras removed at one of seven levels of motion (slow left, medium left, fast left, nootion, fast right, medium right, slow right). Speeds were determined by removing

he line over multiple screen refreshes as follows: no motion = all removed in onecreen, fast = removed in halves over two consecutive screens; medium = removedn thirds over three consecutive screens, and slow = removed in quarters over fouronsecutive screens.

Together with the three alternative cue locations (left, right and none), thereere in total 7 (motion type) by 3 (cue location) = 21 conditions within each block.

hese conditions were randomised and repeated four times over the block of 84 tri-ls with an inter-trial interval of 1 s. Decision times were measured from the initialoint of the line offset, when the first segment was removed using published mil-

isecond timing routines (Hamm, 2001) until the key response was detected usingethods recommended for Turbo Pascal based experiments (Brysbaert, 1990). A

iven threshold does not assume that a motion percept is entirely absent. For exam-le, it is possible that awareness occurs with equal probability for either the realotion or the illusory motion with the other being suppressed from awareness.

he distribution of responses between alternatives would reflect how often a givenignal “wins”. Such a “winner-takes-all” scenario implies that motion is perceivedn all presentations but that the direction of motion cannot be determined withertainty above chance level. This results in a decision time that is an average of theecision time to real only and illusory only motion. Even if opposing real and illu-ory signals cancel, without a clear velocity profile of the illusory motion over thepanned distance, cancelling with real opposing linear motion is unlikely to producepercept of instantaneous presentation, which is the boundary between response

lternatives. However, as shown previously, real linear motion and opposing illusoryotion do interact (Steinman et al., 1995). If the two motion signals are combined

nd cancel, then the expectation would be for the motion signal to shift towardshe decision boundary between the response alternatives, thus yielding increasedesponse times (Cartwright, 1941). The cancellation technique allows us to generatesimple measure to quantify this illusion. In order to ensure that any differences

mplied by the results are due to changes in the illusory motion percept, rather thann the cancellation signal (i.e. the real motion), performance on trials containingnly real motion must also be assessed. The inference that any differences in theancellation process were due to changes in the detection of the illusion, could onlye secured if the real motion detection was also preserved.

Trials in which a participant indicated leftward motion were scored as −1, whilstightward motion was scored as +1. These scores were then averaged over all similarrials to produce a percept score between −1, indicating that consistent leftward

otion was perceived, to +1, indicating consistent rightward motion was perceived.f a given condition resulted in no motion percept, or if the direction was uncertain,hen we predicted an equal distribution between left and right responses, resulting

logia 48 (2010) 3121–3127 3123

in a mean score of 0. Any response bias would be signalled by the deviation fromzero in the ‘no flash’, no motion condition.

Previous research had already established that a peripheral cue (which is knownto trigger exogenous attention) would induce a perception of illusory motion awayfrom the location of the cue in this paradigm (Crawford et al., 2006; Hamm & Klein,2002; Hikosaka et al., 1991, 1993a; Hikosaka, Miyauchi, & Shimojo, 1993b). There-fore we predicted that the left side flash would induce a rightward illusion of motion,and that the right side flash would induce a leftward illusion of motion. If the real andillusory motion were additive, then the scores for the real motion percept shouldvary in relation to the flash condition. The left flash condition should yield morepositive scores reflecting increased rightward motion perception, whilst the rightflash should yield more negative scores. The overall influence of the illusion onmotion perception can be quantified by the area bounded by the left and right flashcurves.

2. Results

2.1. Preliminary analyses

In order to confirm that participants had understood thetask instructions we conducted a preliminary chi-square analysis(Winer, 1971) to determine if the distribution of the responses cor-responded to the direction of the real motion on the real motion (i.e.‘no flash’) trials. This analysis revealed that four of the 45 partici-pants (two controls, two patients) failed to show a reliable influenceof real motion on their response distributions. Visual inspection oftheir data sets revealed that the two patients apparently misunder-stood the instructions and responded to the side of the flash whenit appeared, and so they were randomly responding during the ‘noflash’ trials, while the two control participants appeared to respondrandomly under all conditions, therefore these participants wereexcluded from further analysis.

An analysis on the ‘no flash’ trials was performed to examinethe possibility of a response bias. An inclusive analysis revealed thatthe controls reported a left bias on motion trials overall (M = −0.17)while the patients tended to report more right bias on motion trials(M = 0.26) (t(43) = 2.31, p < 0.05). However, this difference reflecteda response bias that was restricted to the ‘no motion’ trials. Note,that in the absence of any real motion, the saliency of the illusion,as assessed by the distance between the percept scores for no realmotion when there was a left or right flash, did not differ betweenthe groups (t(43) = 0.67, p > 0.05; 1.30 and 1.15), indicating that thepatient group did not have a greater tendency than the controlsto respond towards the flash rather than in the direction of theillusory motion away from the flash. The percept values for controlsand patients can be seen in Fig. 2(column A) below. Decision timedata is shown in Fig. 2(column B). When the analysis was confinedto the movement trials, patients and control did not differ in theirreal motion percept.

Before considering the results from the illusory motion cancel-lation conditions it was crucial to establish whether there was adisparity between the patients and controls in the perception ofthe real motion.1 We therefore examined whether the percept ofthe real motion was similar between the groups, with a measurethat should be free of response bias, by comparing the differencebetween the mean percept score for the right motion trials and left

tation of any changes in the illusory percept scores is ambiguous as such a changemay reflect (1) different illusions being cancelled by equal real motion percepts, (2)equivalent illusions being cancelled by differing real motion percepts, (3) differingillusions being cancelled by differing real motion percepts. Specifically, if a condi-tion or group is shown to have a weaker real motion percept, then this would tendto increase the influence of the illusory line motion.

3124 T.J. Crawford et al. / Neuropsychologia 48 (2010) 3121–3127

Fig. 2. Perception of motion direction scores (Column A) for controls and patients. Positive values indicate rightward motion was perceived more frequently and negativevalues indicate leftward motion was perceived more frequently. Maximum boundary values, if the same response is generated consistently on all trials for a given condition,a ed onT awayo ‘no flo

em

gt+rwrstrdparStcb

2

iFmeafsctstptp

(F(2,86) = 2.69, p > 0.05, ε = 0.816), but a significant flash location bymovement speed interaction (F(12,516) = 11.73, p < 0.05, ε = 0.641).The mean decision time of the groups was significantly different(F(1,43) = 4.63, p > 0.05; 519 ms vs. 589 ms for controls and patients,

re +1 and −1. Square markers indicate the condition where the flash was presenthese conditions should reflect motion perception when both ILM, illusory motionpposite directions. The dashed line with no markers indicates performance on thef ILM. Column B shows the mean decision times for the participants.

ffects of the attentional cues (flash conditions) can be attributedore clearly to the percept of illusory motion.In the current task the response space is bounded by the rectan-

le defined by the levels of real motion (−3 to 3, for slow left througho slow right) and the percept scores (−1 indicating 100% left, and1 indicating 100% right responding, respectively). This creates aesponse space with an area of 12 units, although all measuresere scaled to a proportion of this space between 0 and 1.0. If the

eal and illusory motion interact, then the motion percept scoreshould shift in relation to the laterality of the attentional cue withhe left flash condition producing more positive scores (increasedightward motion perception), while the right flash should pro-uce more negative motion scores (increased leftward motionerception). This would yield a response curve for left flashes thatre shifted towards more positive values, that is, upwards in thisesponse space, generating a larger area under the response curve.imilarly, right flashes should shift the response curve downwardowards more negative values, resulting in a reduced area under theurve. The total strength of the illusion can therefore be quantifiedy the area between the response curves to the left and right flashes.

.2. Perceptual scores and decision times

The motion percept scores for controls and patients are shownn Fig. 2(column A) together with decision time data shown inig. 2(column B). The percept scores, especially at the slowestotion conditions away from the flash, are subject to a ceiling

ffect on performance, resulting in the data being unsuited tonalysis of variance. The area measure, however, does not sufferrom this limitation and so to contrast the effects of the illu-ion, the area between the curves for left and right flashes wasomputed, then analysed with t-tests and further non-parametricests. These analyses revealed that people with schizophrenia

howed a reduced effect of the illusion in comparison to con-rols (t(43) = 2.61, p < 0.05; area 0.37 and 0.23, for controls andatients, respectively, see Fig. 3). Two further non-parametricests were performed on this measure. First, a median split waserformed by ranking the individual areas for all participants

the left, circles indicate the condition where the flash was presented on the right.from the flash, and real motion are presented simultaneously either in the same orash’ condition, which provides a measure of real motion perception in the absence

regardless of group, from smallest to largest, and using chi-squareto determine if the groups were differentially distributed aroundthe 50% rank. This revealed that a larger proportion of the con-trol group were in the lower half (smaller:larger areas 9:17)and fewer patients were in the lower half (smaller: larger areas14:5) than would be expected by chance (�2(1) = 6.72, p < 0.05).The rankings were also significantly different when tested with aMann–Whitney U-test (U(19,26) = 145.5, p < 0.05, corrected for ties;mean ranks 17.7 and 26.9, for the patients and controls, respec-tively).

A 3-way mixed factor ANOVA was performed on the deci-sion time data shown in Fig. 2(column B). Greenhouse Geisser(Greenhouse & Geisser, 1959) epsilon values are reported forconditions that violated the assumption of sphericity, withthe probabilities reported adjusted accordingly. This resultedin a significant effect of movement speed (F(6,258) = 10.30,p < 0.05, ε = 0.753), a non-significant effect of the flash location

Fig. 3. The total strength of the illusion can be quantified by the area between theresponse curves to the left and right flashes. The area between the curves are shownfor the control and patient groups, together with standard error bars.

sycho

riltw

3

dwaAoa2oummiupnli

wsttamsssmtcmtaasmttettthd

ttbaictoacc

T.J. Crawford et al. / Neurop

espectively). There was a significant movement speed by groupnteraction (F(12,516) = 11.73, p < 0.05, ε = 0.641). Neither the flashocation by group interaction (F(2,86) = 1.03, p > 0.05, ε = 0.816); norhe interaction between flash location, movement speed, and groupas significant (F(12,516) = 1.70, p < 0.05, ε = 0.641).

. Discussion

Whether or not people with schizophrenia have a fundamentaleficit in the perception of real motion is unclear from previousork (Chen, Levy et al., 199l; Chen, Palafox et al., 1999; Hong et

l., 2009; Keri, Must, Kelemen, Benedek, & Janka, 2006; Li, 2002).number of studies have reported that in schizophrenia thresh-

lds are raised significantly for the detection of coherent motioncross a large field (Li, 2002; Slaghuis, Holthouse, Hawkes & Bruno,007). Studies based on indirect inferences from the reduced speedf the smooth pursuit eye tracking in schizophrenia have tended tose long stimulus durations that has confounded the percept ofotion perception with oculomotor interactions from the trackingotor component, as Hong et al. (2009) observed. No impairment

n the ability of schizophrenics to perceive real motion was detectedsing the current stimulus conditions. Thus, while the real motionercept remained intact, the disparity between the schizophre-ia and control groups in the curves of motion direction could, at

east in part, be attributed to differences in the perception of thellusion.

This finding has implications for an understanding of theell-known abnormality of smooth pursuit eye tracking in

chizophrenia (Levy, Holzman, Matthysse, & Mendell, 1993). Inheir recent work Hong et al. (2009) attempted to clarify the ques-ion of whether the eye tracking problem can be attributed to

sensory source by obtaining a measure of smooth pursuit eyeovement before and after the early open-loop phase. They dis-

ociated these two stages by varying the duration of the motionignal (Hong et al., 2009). In one condition target motion was pre-ented for a period that reduced the likelihood of eye tracking eyeovement during the early open-loop stage (before processing of

he perceptual feedback) and contrasted this with a long durationondition. The participants with schizophrenia revealed no impair-ent in the short duration condition, when feedback from the eye

racking component could not influence the motion percept. Theuthors argued that motion deficits in the motion percept may beconsequence of impaired smooth pursuit tracking in people with

chizophrenia. This result provided strong support for an impair-ent that emerges as a consequence of a primary failure in eye

racking, rather than a cause, as suggested in previous work. Inhe current study we adopted a similar approach to minimize anyffects of smooth pursuit eye movements in schizophrenia. Sincehe stimulus durations used in our study was approximately 52 ms,he conclusions from the Hong et al. (2009) study can be appliedo the current work. Any effects of smooth pursuit were thereforeighly unlikely to influence perceptual judgements given the briefuration of the target motions in the current experiment.

The shift in the perceptual scores revealed that the presenta-ion of the flash induced a perception of illusory motion away fromhis attentional cue. This perception of the illusion was confirmedy the increased positive values of the motion scores when thettention cue was presented on the left side of the display, and thencreased negative values of the motion scores when the attentionue was presented on the right side of the display. In comparison to

he controls, the participants with schizophrenia revealed a smallerverall change in the perceptual scores, as indicated by the reducedrea between the motion detection curves. In comparison to theontrols, the schizophrenia participants revealed a smaller overallhange in the perceptual scores. Therefore, for the schizophrenia

logia 48 (2010) 3121–3127 3125

group the illusory motion appears to only weakly modulate thereal motion percept.

When illusory motion is in competition with an inverse realmotion signal, a weak detection of real motion would be expectedon the basis of the competition for attention. In a winner-takes-all mode, the more salient signal would be expected to win thecompetition, while the weaker signal is disregarded. If people withschizophrenia have difficulty in the integration and distribution ofattention, then the weakest signal would be disregarded accord-ing to the winner-takes-all process. Thus when the illusion andreal motion were placed in conflict, by presenting the direction ofthe real motion towards the attention cue, two possible situationscould have arisen. First, the two motion signals could have con-flicted to generate mutual inhibition, resulting in a more difficultdecision for the participant. Alternatively, the final perception maybe based upon a “winner-takes-all” race where either the illusorymotion or the real motion is perceived and the weaker signal simplydisregarded. Both possibilities could explain the perceptual data,with the first situation suggesting that people with schizophre-nia experience a weaker inhibition, not because the illusion is notdetected, but because it is an illusory signal that it is perceived witha duration that was too short (i.e. too fast) to cancel the real motion.The second situation suggests that the illusion wins less frequently,implying that the illusion produces an unreliable signal for patientsin comparison to the controls. However, the decision time data canhelp to distinguish between the two possibilities, and as we outlinebelow, is more consistent with the former suggestion.

In the situation where there was no real motion AND no illu-sory motion (no attention cue), decision times for both controlsand patients were long, indicating the need to guess rather thanto respond on the basis of an ambiguous signal. This was expectedsince the ‘no motion’ condition was the boundary between the illu-sory and real motion condition; boundary conditions are knownto yield slow responses (Cartwright, 1941). When real motion waspresented in isolation (i.e. the motion with no flash) response timesare short, and with decreasing response times as the motion slows,consistent with the condition moving further from the region ofambiguity (Cartwright, 1941). Similarly, when only the illusorymotion was presented (i.e. flash with no real motion), responsetimes were relatively short. In other words, when participantsresponded on the basis of either the real motion percept or illu-sory motion, their response times were short, in comparison to thecondition in which responses were based upon ambiguous signals.In the flash (attention cue) conditions, decision times tended tobe longer at the conditions where perceptual scores are near zero(although this was not apparent in the patient right flash condition).This tendency for response times to increase at the point where thepercept score approaches zero suggests that the signal is becom-ing more ambiguous as responses approach a boundary condition(Cartwright, 1941) as in the no motion trials. A “winner-takes-all”model, predicts that response times should be relatively short andirrespective of the direction of motion. The controls generated shortresponse times in the conditions when the direction of the illusionand the real motion were congruent, suggesting that the motionsignals were additive and hence the response times became faster(see Fig. 2B). Although the role of other factors, such as alertness,cannot be entirely eliminated, the fact that the decision times weremodulated in relation to the ‘no flash’ condition, depending uponwhether the illusion was in the same or opposite direction as thereal motion, strongly suggests that that the illusory motion signaldirectly influenced these response times. Schizophrenic patients

showed less influence of the illusion on their decision times, whichis consistent with the idea that the illusion produced a weaker effect(perhaps due to a shorter illusory motion signal).

The patients appeared to perceive the illusion with a shorterduration than the controls. The performance on the pure ILM trials

3 sycho

(gscagtat

mttKTc2Ldn

ptldcwiogaehmAwtMsaioodariegipotp

Emattppiwwt

126 T.J. Crawford et al. / Neurop

flash with no real motion) did not differ between the groups, sug-esting the motion signals were equally salient. However, for thechizophrenic patients a faster real motion signal was required toancel ILM, as the reduced area indicates the left and right curvesre closer together. The faster illusion may be a result of a shallowerradient spreading outward from the peripheral cue than the con-rol participants. Whether this shallower gradient is specific to thettentional processes, pre-attentional processes, or both, remainso be determined.

There is growing and compelling evidence that visual attentionodulates various aspects of visual performance including reaction

imes (Posner, 1980), improved discrimination of the properties ofhe attended stimulus, such as its orientation (Downing, 1988; Lee,och, & Braun, 1997) and contrast sensitivity (Carrasco et al., 2000).he neural effects of visual attention are reflected in increases inortical neural activity (e.g. Carrasco et al., 2000; Reynolds et al.,000) and reduction in distracter interference or noise (Dosher &u, 2000). What and how we see is determined not only by the rawata that arrives at the sensory receptors, but also by whether orot we attend to these sense data.

Recently, Turatto, Vescovi, and Valsecchi (2007) provided com-elling evidence that attention also influences the perception ofhe speed of movement. In both the natural world with manyife-threatening predators and, our modern world of potentiallyangerous vehicles, the ability to perceive and track motion is cru-ial to survival. Indeed the motion percept is so compelling thate are vulnerable to various illusions of motion. A clear example

s the ILM described above. However, the source of this illusionf motion is not fully understood and there are a number of sug-ested mechanisms. It has been suggested that the illusion emergess the result of a gradient of exogenous visual attention (Hikosakat al., 1991, 1993a; Schmidt & Klein, 1997). The attentional gradientypothesis runs as follows: first, the luminance attention cue auto-atically attracts attention to its location in space (Posner, 1980).ttention is then distributed as a gradient centred at this location,ith a decline in attentional benefits with increasing distance from

he centre (Laberge & Brown, 1986; Muller & Kleinschmidt, 2004;uller, Mollenhauer, Rosler, & Kleinschmidt, 2005). The focus of

patial attention receives the benefits of prior entry (Hikosaka etl., 1993b; Shore, Spence, & Klein, 2001), such that an objects thats presented at the attended location is perceived more rapidly thanne at a non-attended location. Thus, attention also modulates therder in which visual events are processed. In the context of the ILMisplay, attention is drawn to the attention cue, which sets up anttentional gradient emanating from this location. When the bar isemoved (or presented), the terminal endpoint of the bar that liesn the vicinity of the attentional cue falls into the region that ben-fits from prior entry, with the remainder of the bar falling along aradient of these benefits, and therefore will be subject to increas-ng delays of visual processing. This cumulative series of effectiveerceptual offsets (or onsets), yields the perceptual phenomenonf a bar in motion away from the attention-cued location. In addi-ion this illusory motion itself can attract attention away from aeripheral stimulus (Crawford et al., 2006).

Eriksen and his co-workers (see Eriksen & St. James, 1986;riksen & Yeh, 1985) have popularised the zoom lens metaphorodel of visual attention. According to Eiksen, attention may oper-

te effectively in the mode of a wide-angle view camera, wherehe resolution of visual attention is relatively weak and widely dis-ributed across the visual field. This would enable the fast, parallelrocessing of visual items. When attention zooms in to a narrow

ortion of the visual field, the resolving power increases for visual

tems within that spatial area. The model accounts for conditions inhich attention is distributed in parallel to multiple locations buthere the ‘resolution’ is low for specific items within the atten-

ional field. The model also explains conditions where attention

logia 48 (2010) 3121–3127

can focus narrowly at a specific item, when the resolution is high,but for a restricted portion of the visual field. Here serial scanning,using, for example, a series of saccadic eye movements to selectitems, would generate an increase in the cost of the search timesfor multiple items. However, whether or not attention is focused ona spatially limited region or distributed in a more shallow form inparallel depends on the nature of the visual task. Healthy observershave a flexible attentional focus, that will adjust to the nature ofthe task. This may be an important distinguishing. In schizophre-nia the focusing operation appears to be less flexible, giving riseto a visual attention system that yields excessively intense per-cepts and abnormal concepts. Such a process may explain clinicalreports of enhanced sensations, while simultaneously protectingpatients from perceptual illusions that are dependent on a flexi-ble attentional network. In the current work ILM has uncovered anattentional property which may protect schizophrenics from someof the perceptual distortions of visual illusions and provides a novelapproach to probing visual attention in this disorder.

Over 90% of cells in primary visual cortex (V1) are subject toinhibitory activity from their neighbouring cells (Jones, Grieve,Wang, & Sillito, 2001). There is a growing view that schizophre-nia is a disorder of disconnected neural networks. For example,people with schizophrenia show a clear reduction in the nor-mal enhancement of spatial orientation detection when the targetwas presented alongside similarly orientated flanker stimuli (Must,Janka, Benedek, & Keri, 2004), supporting the idea of a disruption inlateral connectivity in early vision processing in V1. The change inthe attentional gradient may therefore reflect abnormal intercon-nectivity within the schizophrenic brain at a number of levels in avisuo-attentional network.

4. Conclusion

In the current work we demonstrate the effect in schizophre-nia of ‘real’ motion on the perception of this attention-inducedillusion of motion. The current results are indicative of a shallowattentional gradient in schizophrenia. Whilst this attentional prop-erty is sufficient to detect real and illusory motion when presentedin isolation, there are clear limitations when motion signals arecombined. However, the results will require replication with largersamples and alternative methods for addressing the possibility ofresponse bias.

Acknowledgement

This work was funded by the New Zealand Foundation forResearch, Science & Technology (MK & TC) LANC0401 TC is sup-ported by Sir John Fisher Foundation, UE is supported by DFG grantET 31/2-1. We are grateful to 2 anonymous reviewers for theirhelpful comments.

References

Andreasen, N. C. (1984). Scale for the assessment of positive symptoms (SAPS). IowaCity: University of Iowa.

Andreasen, N. C. (1983). Scale for the assessment of negative symptoms (SANS). IowaCity: University of Iowa.

Bleuler, E. (1950). Dementia praecox or the group of schizophrenias. New York: Inter-national Universities Press. (J. Zinkin, Trans.).

Brysbaert, M. (1990). A warning about millisecond timing in Turbo Pascal. BehaviorResearch Methods, Instruments, & Computers, 22, 344–345.

Cartwright, D. (1941). Relation of decision time to the categories of response. Amer-ican Journal of Psychology, 54, 174–196.

Chen, Y., Levy, D. L., Nakayama, K., Matthysse, S., Palafox, G., & Holzman, P. S. (1999).Dependence of impaired eye tracking on deficient velocity discrimination inschizophrenia. Archives of General Psychiatry, 56, 155–161.

Chen, Y., Palafox, G. P., Nakayama, K., Levy, D. L., Matthysse, S., & Holzman, P. S.(1999). Motion perception in schizophrenia. Archives of General Psychiatry, 56,149–154.

sycho

C

C

D

D

D

D

E

E

F

G

H

H

H

H

H

H

H

I

J

J

T.J. Crawford et al. / Neurop

arrasco, M., Penpeci-Talgar, C., & Eckstein, M. (2000). Spatial covert attentionincreases contrast sensitivity across the CSF: Support for signal enhancement.Vision Research, 40, 1203–1212.

rawford, T., Kean, M., Klein, R. M., & Hamm, J. P. (2006). The effects of illusory linemotion on incongruent saccades: Implications for saccadic eye movements andvisual attention. Experimental Brain Research, 173, 498–506.

akin, S., Carlin, P., & Hemsley, D. (2005). Weak suppression of visual context inchronic schizophrenia. Current Biology, 15, R822–824.

iefendorf, A. R., & Dodge, R. (1908). An experimental study of the ocular reactionsof the insane from photographic records. Brain, 31, 451–489.

osher, B. A., & Lu, Zhong-Lin. (2000). Mechanisms of perceptual attention in pre-cuing of location. Vision Research, 40, 1269–1292.

owning, C. J. (1988). Expectancy and visual–spatial attention: Effects on perceptualquality. Journal of Experimental Psychology: Human Perception and Performance,14, 188–202.

riksen, C. W., & Yeh, Y. (1985). Allocation of attention in the visual field. Journal ofExperimental Psychology: Human Perception & Performance, 11, 583–597.

riksen, C. W., & St. James, J. D. (1986). Visual attention with and around thefield of focal attention: A zoom lens model. Perception & Psychophysics, 40(4),225–240.

irst, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1997). Structured clinicalinterview for DSM – IV axis I disorders. Washington, DC: American PsychiatricPress Inc.

reenhouse, S. W., & Geisser, S. (1959). On methods in analysis of profile data.Psychometrika, 24, 95–112.

amm, J. P. (2001). Object-oriented millisecond timers for the PC. Behavior ResearchMethods Instruments & Computers, 33, 532–539.

amm, J. P., & Klein, R. M. (2002). Does attention follow the motion in the “shootingline” illusion? Perception & Psychophysics, 64, 279–291.

eathcote, A. (1988). Screen control and timing routines for the IBM microcomputerfamily using a high-level language. Behavior Research Methods, Instruments andComputers, 20, 289–297.

ikosaka, O., Miyauchi, S., & Shimojo, S. (1991). Focal visual attention producesmotion sensation in lines. Investigative Opthalmology & Visual Science, 32, 716.

ikosaka, O., Miyauchi, S., & Shimojo, S. (1993a). Focal visual attention producesillusory temporal order and motion sensation. Vision Research, 33, 1219–1240.

ikosaka, O., Miyauchi, S., & Shimojo, S. (1993b). Voluntary and stimulus-inducedattention detected as motion sensation. Perception, 22, 517–526.

ong, L. E., Turano, K. A., Hugh, B., O’Neill, H. B., Hao, L., Wonodi, I., et al. (2009).Is motion perception deficit in schizophrenia a consequence of eye-trackingabnormality? Biological Psychiatry, 265, 1079–1085.

lg, U. J., & Their, P. (2008). The neural basis of smooth pursuit eye movements in therhesus monkey brain. Brain and Cognition, 68, 229–240.

ancke, D., Chavane, F., Naarman, S., & Girinvald, A. (2004). Imaging cortical correlatesof illusion in early visual cortex. Nature, 428, 423–426.

ones, H. E., Grieve, K. L., Wang, W., & Sillito, A. M. (2001). Surround suppression inprimate V1. Journal of Neurophysiology, 86, 2011–2028.

logia 48 (2010) 3121–3127 3127

Keri, S., Must, A., Kelemen, O., Benedek, G., & Janka, Z. (2006). Development of visualmotion perception in children of patients with schizophrenia and bipolar disor-der: A follow-up study. Schizophrenia Research, 82, 9–14.

Kraepelin (1919). Dementia Praecox and Paraphrenia (R.M. Barclay, Trans., 1971).Laberge, D., & Brown, V. (1986). Variations in size of the visual-field in which tar-

gets are presented – An attentional range effect. Perception & Psychophysics, 40,188–200.

Lee, D. K., Koch, C., & Braun, J. (1997). Spatial vision thresholds in the near absenceof attention. Vision Research, 37, 2409–2418.

Levy, D. L., Holzman, P. S., Matthysse, S., & Mendell, N. R. (1993). Eye tracking dys-function and schizophrenia: A critical perspective. Schizophrenia Bulletin, 19,461–536.

Li, C. S. R. (2002). Impaired detection of visual motion in schizophrenia patients.Progress in Neuro-Psychopharmacology & Biological Psychiatry, 26, 929–934.

McGhie, A., & Chapmann, J. (1961). Disorders of attention and perception in earlyschizophrenia. British Journal of Medical Psychology, 34, 103–116.

Muller, N. G., & Kleinschmidt, A. (2004). The attentional ‘spotlight’s’ penumbra:Center-surround modulation in striate cortex. Neuroreport, 15, 977–980.

Muller, N. G., Mollenhauer, M., Rosler, A., & Kleinschmidt, A. (2005). The attentionalfield has a Mexican hat distribution. Vision Research, 45, 1129–1137.

Must, A., Janka, Z., Benedek, G., & Keri, S. (2004). Reduced facilitation effect ofcollinear flankers on contrast detection reveals impaired lateral connectivity inthe visual cortex of schizophrenia patients. Neuroscience Letters, 357, 131–134.

Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychol-ogy, 32, 3–25.

Reynolds, J. H., Pasternak, T., & Desimone, R. (2000). Attention increases sensitivityof V4 neuron. Neuron, 26, 703–714.

Schmidt, W. C., & Klein, R. M. (1997). A spatial gradient of acceleration and temporalextension underlies three illusions of motion. Perception, 26, 857–874.

Shore, D. I., Spence, C., & Klein, R. M. (2001). Visual prior entry. Psychological Science,12, 205–212.

Slaghuis, W. L., Holthouse, T., Hawkes, A., & Bruno, R. (2007). Eye movement andvisual motion perception in schizophrenia II: Global coherent motion as a func-tion of target velocity and stimulus density. Experimental Brain Research, 182,415–426.

Structured Clinical Interview for DSM-IV Axis I Disorders (2010). Clinician Version(SCID-CV).

Steinman, B. A., Steinman, S. B., & Lehmkuhle, S. (1995). Visual attention mechanismsshow a centre-surround organization. Vision Research, 35, 1859–1869.

Turatto, M., Vescovi, M., & Valsecchi, M. (2007). Attention makes moving objects beperceived to move faster. Vision Research, 47, 166–178.

vonGrunau, M., Dube, S., & Kwas, M. (1996). Two contributions to motion induction:A preattentive effect and facilitation due to attentional capture. Vision Research,36, 2447–2457.

vonGrunau, M., Racette, L., & Kwas, M. (1996). Measuring the attentional speed-upin the motion induction effect. Vision Research, 36, 2433–2446.

Winer, B. J. (1971). Statistical principles in experimental design (2nd ed.). McGraw-Hill.