R

Attention and Masking in SchizophreniaLaurence Lalanne, André Dufour, Olivier Després, and Anne Giersch

Background: Patients with schizophrenia are known to be impaired in masking tasks, but the mechanisms underlying their deficits are stillelusive. Our study was intended to examine attentional effects, which have a known impact on masking in healthy volunteers but have onlyrarely been explored in relation to masking in patients.

Methods: We compared focused versus divided attention in 18 control subjects and 18 patients using forward and backward maskingtasks. In the conventional masking task, subjects had to locate one target among four possible locations. Presentation of one target allowsattention to be focused, in contrast with the divided attention task in which two targets were presented either in the same hemifield ordifferent hemifields.

Results: Our results reproduce patients’ deficits in forward and backward masking tasks but only when one target is presented. We showthat control subjects benefit from focused attention, much more so than patients. Furthermore, patients’ performance is identical to that ofcontrol subjects in backward masking when targets are presented across hemifields. This performance equalization was checked to ensureit was not due solely to the redundancy of signals (two vs. one). We achieved this by comparing performance when two targets werepresented in the same vs. across hemifields, the latter yielding a greater redundancy gain.

Conclusions: From the results, it is unlikely that redundancy can account for the whole pattern of results, which suggest instead thatattention deficits play a role in backward masking impairments in patients.

pdtt“ssistticttoumgic

bbti(bpmedtelojs

Key Words: Backward masking, divided attention, focused atten-tion, forward masking, redundancy gain, schizophrenia

P atients with schizophrenia consistently display deficits in vi-sual masking tasks (1– 4). This particular deficit is related nei-ther to intellectual deterioration (5) nor to neuroleptics (6,7).

Several authors have proposed that it reflects vulnerability toschizophrenia (8,9) and has an impact on social outcome (10). Theseresults suggest it reveals a key impairment in patients, hence theneed to gain a better understanding of its underlying mechanismsand significance. The role of attention has been shown repeatedlyin respect of backward masking (11), and attention impairmentshave been widely described in patients with schizophrenia (12,13).However, the impact of attention on masking paradigms has rarelybeen explored in patients. In our study, we wished to determine theextent to which patients with schizophrenia were still impairedwhen their attention could not be focused on a single target, andwe controlled for a possible confounding factor, the redundancygain.

In visual masking paradigms, a target (usually a letter or symbol)is presented briefly in quick succession with a mask. The subject isinstructed to identify or localize the target, the visibility of which islessened by the mask. The mask is displayed either before or afterthe target (forward or backward masking tasks). Mask and target areseparated by a stimulus onset asynchrony (SOA), the duration ofwhich is manipulated. Patients with schizophrenia need largerasynchronies between target and mask to reach a performancelevel equivalent to control subjects (1– 4). Mechanisms that are

From U666 (LL, AG), National Institute for Health and Medical Research;Department of Psychiatry I (LL, AG), University Hospital of Strasbourg;Mixt Unit of Research UMR7237 (AD, OD), National Center for ScientificResearch, Laboratory of Imaging and Cognitive Neurosciences, Univer-sity of Strasbourg, Strasbourg, France.

Address correspondence to Anne Giersch, M.D., Ph.D., INSERM U666; CentreHospitalier Régional Universitaire de Strasbourg, Département de Psy-chiatrie I, Hôpital Civil, 1, Place de l’Hôpital, F-67091 Strasbourg, Cedex,France. E-mail: giersch@alsace.u-strasbg.fr.

peceived May 27, 2011; revised Sep 1, 2011; accepted Sep 10, 2011.

0006-3223/$36.00doi:10.1016/j.biopsych.2011.09.018

roposed as an explanation for the impairment in patients areerived from theories that account for masking in healthy volun-

eers. Masking is a phenomenon traditionally attributed to interac-ions between neural visual channels known as “transient” andsustained” channels (14 –18). The transient channel responds totimulation quickly and briefly and conveys information of lowpatial and high temporal frequency, that is, transient and globalnformation. In contrast, the sustained channel responds morelowly and to high spatial frequencies and underlies stimulus iden-ification and fine-scale analysis. These systems correspond, respec-ively, to the magnocellular and parvocellular visual pathways andnteract in complex ways, depending on the type of masking pro-edure. Backward masking in healthy volunteers is usually believedo involve both integration and interruption mechanisms. Integra-ion is defined as a fusion between the target and the mask relyingn the integration of the sustained activities elicited by both stim-li, and it occurs primarily at short SOAs (maximal between 0 and 30sec). Interruption, on the other hand, is believed to occur at lon-

er SOAs (maximal between 50 to 100 msec), when the transientnformation conveyed by the mask “interrupts” the sustained pro-essing of the target, thus reducing its visibility (11,14).

On this basis, several hypotheses, not mutually exclusive, haveeen proposed to explain schizophrenia patients’ impairments inackward masking. One influential hypothesis, based on studies

hat evaluated the detection of low versus high spatial frequencynformation, suggests a deficit at the level of the transient channel6,19), which, if impaired, would mean target processing would note interrupted as efficiently. Consequently, the first stimulus wouldersist longer and would be merged with the mask via integrationechanisms (20). However, this hypothesis alone may not be

nough to explain the entire pattern of deficits observed in patientsuring masking tasks. Rassovsky et al. (21) used meta- and paracon-

rast to show that masking deficits are still observed in patientsven when the mask location does not overlap with the target

ocation, such that mask and target cannot be fused in space. Effectsbserved in metacontrast and paracontrast are explained by “ob-

ect substitution,” which might also account for the deficits ob-erved in patients. It is a theory based on common views of visual

erception, in which object identification requires not only feedfor-

BIOL PSYCHIATRY 2012;71:162–168© 2012 Society of Biological Psychiatry

(tsmrTtsottwsctptifts

tsblmftpdatdnppsatdtwbci

dthwssefitahmps

jstvthi(awatrttettf

M

L. Lalanne et al. BIOL PSYCHIATRY 2012;71:162–168 163

ward processing but also feedback connections to overcome anyambiguity between the different interpretations that may be de-rived from the initial feedforward processing (22). With masking,both the target and the mask would elicit feedforward and feed-back processing in turn. However, the target and the mask arepresented in close spatiotemporal proximity. This means a possiblemismatch between feedforward and feedback processing. For ex-ample, in backward masking, when the target has disappeared andthe mask is displayed, the feedforward processing would corre-spond to the mask, whereas the feedback would correspond to thetarget. It would lead to the target being substituted by the mask,before all ambiguities about the target have been overcome. Itmight account for patients’ deficits if the target processing is tooweak or the mask too strong. However, like the hypothesis withrespect to excessive integration, this theory must also account forresults in implicit tasks that show patients are very sensitive to shortduration information, even when efficiently masked. Herzog et al.(23) explored the incidental influence of short-duration stimuli onperformance in a masking task. They used a 20-msec prime andfound that patients were as sensitive to such short-duration stimulias control subjects. Del Cul et al. (24) also showed that the implicitprocessing of the target was preserved. On the whole, the results ofthe latter studies show the typical increase in backward masking inpatients, which, however, does not seem to be systematically asso-ciated with the target and the mask fusing at an early level ofprocessing and still allows the target to be processed efficiently.

As proposed in several models (25), attention is important forenabling information to reach consciousness. Furthermore, the lat-est “object-substitution” theory stresses the importance of feed-back connections that may be reinforced through attention. In fact,studies on object substitution have been particularly helpful inhighlighting how attention influences metacontrast (26,27) andeven backward masking (28). In addition, attention effects havefrequently been described in patients with schizophrenia (29 –31),especially with respect to visual perception (13,32), although fewstudies have confirmed its role in masking deficits in patients withschizophrenia. Granholm et al. (33) assessed how attentional re-sources are allocated during backward masking tasks by measuringpupil dilation. They suggested that patients either failed to allocatesufficient resources or that they mistakenly allocated them towardthe mask instead of the target. This would be consistent with theliterature suggesting selection control deficits (34). Rassovsky et al.35) manipulated attention by warning subjects before a subset ofrials that they would receive a monetary reward for a good re-ponse. Although this manipulation improved patient perfor-

ance, the effect was fairly modest. In all experiments, patientsemained impaired in relation to control subjects in all conditions.he hypothesis that attention influences backward masking in pa-ients warrants further examination. We made no attempt in ourtudy to improve masking performance by manipulating attentionr to measure attention alongside the masking task. Rather, we

ried to minimize the impact of attention in the masking procedureo see whether the performance of patients and control subjectsould then be equated. We reasoned that attention allocation

hould be efficient, at least in healthy control subjects, when fo-used on a single target but not when divided between two loca-ions. If attention has a role to play in the masking deficit found inatients, their performance should be more similar to that of con-

rol subjects when attention is divided. We therefore checked thempact of attention by comparing performance when attention isocused on a single target versus when it is divided between twoargets. In the divided-attention condition, two targets were pre-

ented, which means a possible redundancy gain in which detec- s

ion is facilitated by comparison of two identical stimuli with aingle one (36,37). Despite this, attention focalization predictedetter performance when there was only one target. We predicted

ess attention focalization efficiency in patients, with similar perfor-ance for one versus two targets. However, another explanation

or this could be an effect on the redundancy gain, and we wantedo determine whether this gain was affected in patients. Our ap-roach was based on recent studies suggesting that the redun-ancy gain might be affected in a paradoxical way in presentationcross hemifields. Indeed, several studies have demonstrated thathe redundancy gain is greater in detection tasks when signals areisplayed across hemispheres than when the same number of sig-als is displayed within hemifields (38,39). Underlying this at least inart is the fact that bilateral stimuli activate both hemispheres inarallel: bilateral activation would help detection and motor re-ponse more than unilateral activation (38). This means that inddition to the redundancy gain due to the presentation of twoargets instead of only one, the presentation of the two targets inifferent hemifields should result in even further detection facilita-

ion (38, 39). This effect might be paradoxically enlarged in patientsith schizophrenia because of interhemispheric transfer distur-ances. When interhemispheric transfer is disturbed, as in cases ofommissurotomy or callosal agenesis (40,41), redundancy gain is

ncreased. This is also the case in schizophrenia (42).This might have a number of implications for the masking para-

igm because in the typical paradigm, the mask includes informa-ion displayed in both hemifields, implying the activation of bothemispheres. If the redundancy gain was increased in patients, itould mean a higher impact for the mask in patients than in control

ubjects. However, the presentation of two rather than one targethould help patients more than control subjects. This should bespecially when the two targets are presented in different hemi-elds. To confirm this, we contrasted a condition in which bothargets are presented in the same hemifield with one in which theyre displayed in different hemifields. If the redundancy gain isigher in patients than control subjects and accounts for perfor-ance variations across tasks, patients’ performance should im-

rove more than that of control subjects when targets are pre-ented across hemifields rather than within the same hemifield.

Our predictions were as follows. First, in healthy control sub-ects, the possibility of focusing attention in the single target pre-entation should lead to better performance than when there arewo targets. Focused attention may help to amplify the signal con-eyed by the target, thus helping to avoid substitution or interrup-ion of target processing by the mask. Inasmuch as these effectsave been observed mainly in metacontrast and backward mask-

ng, we expected them to be less pronounced in forward masking11,28). If patients have difficulty related to focused attention, thedvantage of having a single target should be lessened, especiallyith backward masking. Furthermore, by comparing performance

s a function of within-hemifield and between-hemifield presenta-ion, we were also able to check the advantage provided by theedundancy of signals across hemifields and to establish whetherhere was a differential effect of mask and target redundancy be-ween groups. If patients benefit from an increased redundancyffect, their performance should improve more than that of con-rols when targets are presented in different hemifields as opposedo the same hemifield. This should be true in both backward andorward masking.

ethods and Materials

Demographic characteristics of the 18 patients and 18 control

ubjects are displayed Table 1. It should be noted that the patients’

www.sobp.org/journal

mm

R

trogasfmAe

S

8mt

D

epcwafb

swrwlIip

164 BIOL PSYCHIATRY 2012;71:162–168 L. Lalanne et al.

group is fairly asymptomatic. Details on participants (diagnosis,exclusion criteria, and ethics) and on the apparatus can be found inSupplement 1.

StimuliIn all tasks subjects were instructed to locate target stimuli

(squares .8° � .8°, luminance 3.26 cd/m2), which could be displayedin four possible locations (in the four corners of a virtual square (5.5° �5.5°) around a central fixation point. The single masking task corre-sponded to the traditional masking experiment in which a singletarget is presented for 33 msec and randomly assigned to one of thefour locations (top right or left, or bottom right or left).

In the double masking task, two target stimuli were presentedfor 33 msec either in different hemifields or within the same hemi-field. The pairs of squares were displayed either at the top, bottom,or left or right side of the center of the screen. Stimuli were followedor preceded by a mask, defining backward and forward masking,respectively. The mask was presented for 33 msec at a luminance of3.26 cd/m2 on a black background of .02 cd/m2, with four whitesquares superimposed on the four target locations.

ProcedureThe order of the two masking tasks (single vs. two target stimuli)

was counterbalanced across subjects in each group. The procedureis illustrated in Figures 1 and 2 and is detailed in Supplement 1.Eleven SOAs were used with values between �250 msec (forward

Table 1. Demographic and Clinical Data of the Participants

Patients Control Subjects

Sex (Male/Female) 11/7 11/7Age (mean � SD) 35.7 � 6.3 34.3 � 6.4Education (years, mean � SD) 11.8 � 2 12.5 � 1.8Medication (typical/atypical) 4/14 —Dose of Chlorpromazine Equivalents 253 mg/day —PANSS Positive Symptoms (mean � SD) 15.4 � 4 —PANSS Negative Symptoms (mean � SD) 19 � 7.3 —PANSS General Symptoms (mean � SD) 35.8 � 12.8 —PANSS Total (mean � SD) 70.3 � 21.2 —

PANSS, Positive and Negative Syndrome Scale.

www.sobp.org/journal

asking) and �250 msec (backward masking) and including 0sec (in which case, only the mask was visible).

esults

We first analyzed separately the results in the different maskingasks. This was done to check whether we replicate the typicalesults from the literature. For each task, we conducted an analysisf variance (ANOVA) on correct responses with group as a between-roup variable and with type of masking (backward vs. forward)nd SOAs as within-group variables. We add the partial eta2 (effectize). Note that we had to exclude the SOA � 0 when comparingorward and backward masking. We decomposed interactions by

eans of Tukey post hoc analyses, completed in some cases byNOVAs on a restricted number of conditions—for example, onach SOA.

ingle Masking TaskThe global analysis of variance showed a group effect [F (1,34) �

.9, p � .01, partial �2 � .21), with patients making globally 15.5%ore errors than control subjects, but no interaction with SOA or

ype of masking (Figure 3).

ouble Masking TaskSquares Presented in the Same Hemifield. There was an

ffect of the type of masking presentation [F (1,34) � 6, p � .05,artial �2 � .15], with an increase of errors by 4% in backwardompared with forward presentation (Figure 4, left panel). Thereas no significant effect of group even when considering forward

nd backward masking separately [F (1,34) � 2.7, ns, partial �2 � .07or forward masking and F (1,34) � 1.8, ns, partial �2 � .05 forackward masking).

Squares Presented in Different Hemifields. The ANOVAhowed an interaction between group and masking type (back-ard vs. forward) [F (1,34) � 6.1, p � .05, partial �2 � .15; Figure 4,

ight panel]. Performance was then analyzed separately in back-ard and forward masking. Patients and control subjects had simi-

ar performance in backward masking task (F � 1, partial �2 � .003).n forward masking, however, the analysis showed a significantnteraction between SOA and group [F (4,136) � 3.9, p � .005,artial �2 � .1). Decomposing this interaction by means of the

Figure 1. This figure depicts the time course of a forwardmasking task in which subjects locate the single target,which is presented after the mask. Each trial began withthe presentation of the central fixation point and fourempty squares. Subjects first had to fixate the centralpoint for 500 msec, as checked by continuous eye track-ing. The mask was displayed first, followed by the target,which was represented by the filling in of one square.After the mask and targets had disappeared, emptysquares remained on the screen until subjects respondedby hitting one of four keys arranged to match the targetlocations: top left, top right, bottom left, and bottomright. The procedure is the same in backward masking,except that the mask is presented after the target insteadof before. SOA, stimulus onset asynchrony.

p

C

cthoat

B

s5

i

Wtph

tTat(wt

ptabibh

aa.sth

Gwiciyn

F

ip

L. Lalanne et al. BIOL PSYCHIATRY 2012;71:162–168 165

Tukey post hoc analysis did not show any significant effect. OnlyANOVAs performed on each SOA showed an impairment for thetwo largest SOAs at 200 msec and 250 msec [by 18%, F (1,34) � 5.99,p � .05, partial �2 � .15 at 200 msec, and by 21.7%, F (1,34) � 9.2,

� .01, partial �2 � .21 at 250 msec].

omparison Between Masking ConditionsThe differences in performance observed in the various masking

onditions were confirmed in a global analysis with group as be-ween-group variable and the type of task (double masking intra-emifield, double masking interhemifield, single masking), the typef masking (forward vs. backward), and SOAs as within-group vari-bles (Figure 5). The analysis showed a significant interaction be-ween the four variables [F (8,272) � 2, p � .05, partial �2 � .06).

ackward MaskingThe analysis restricted to data on backward masking showed a

ignificant interaction between the type of task and group [F (2,68) �.2, p � .01, partial �2 � .13), and there was a significant effect of

the type of task in each group [F (2,34) � 25, p � .001, partial �2 � .6n controls and F (2,34) � 6.6, p � .005, partial �2 � .28 in patients].

Figure 3. Rate of correct responses as a function of stimulus onset asynchro-

8nies (SOAs; msec) when only one square is presented in forward (SOAsbelow 0 msec) and backward (SOAs � 0 mecs) masking condition.

e first compared performance in tasks with one versus two targetso check the effects of attention focalization. We then comparederformance in tasks with two targets in the same versus in twoemifields to check the effect of redundancy gain.

One Target Versus Two: Attention Focalization. Followinghe effect of the type of task in control subjects (discussed earlier),ukey post hoc analyses showed that performance was better withsingle target, compared with when there were two targets 1) in

wo hemifields (by 15.7%, p � .001) or 2) within the same hemifieldby 19%, p � .001; Figure 5, left panel). Similar results were observed

ith ANOVAs comparing performance with one target and twoargets (either in the same or in different hemifields).

The advantage provided by the single target was not as clear inatients (Figure 5, right panel). Tukey post hoc analyses showed

hat performance improved significantly in patients when there wassingle target rather than two targets in the same hemifield, but onlyy 9.8% (p � .05). This improvement was larger in control subjects than

n patients, as confirmed by a sub-ANOVA showing an interactionetween type of task (one single target vs. two targets in the sameemifield) and group [F (1,34) � 4.2, p � .05, partial �2 � .1].

When comparing performance in the task with a single targetnd two targets in two different hemifields with a Tukey post hocnalysis, there was no difference in patients (45.7% vs. 46.9%, p �

7). This again differed significantly from the improvement ob-erved in controls, as shown by a sub-ANOVA showing an interac-ion between type of task (one single target vs. two targets in twoemifields) and group [F (1,34) � 9.4, p � .005, partial �2 � .22).

Two Targets in Two Hemifields Versus One: Redundancyain. Both patients and control subjects’ performance improvedhen the two targets were displayed in two hemifields rather than

n one unique hemifield (Figure 5), although this effect was signifi-ant only in patients [F (1,17) � 8.5, p � .01, partial �2 � .33) and not

n control subjects [F (1,17) � 2.6, ns, partial �2 � .13]. This did notield any interaction between type of task and group [F (1,34) � 1.4,s, partial �2 � .04).

orward MaskingThe subanalysis restricted to forward masking showed a significant

nteraction among the type of task, SOAs, and group [F (10,340) � 2.2,� .05, partial �2 � .06).

Controls’ performance globally varied with the task [F (2,34] �

Figure 2. This figure depicts the time course of a back-ward masking task in which two targets are presented atthe top, bottom, or left or right side of the screen center.The procedure is identical to the one used with one singletarget, except that subjects have to locate a pair of targetsrather than one single target. They respond by hitting oneof four keys arranged to match the locations of the tar-gets. This description holds for forward masking, exceptthat the mask follows rather than precedes the targets.SOA, stimulus onset asynchrony.

.6, p � .001, partial �2 � .33] but not with SOAs (F � 1, partial �2 �

www.sobp.org/journal

fwewt

efi

oi

mht

I

iepd

D

miisii

166 BIOL PSYCHIATRY 2012;71:162–168 L. Lalanne et al.

.04, Figure 5 left panel). Tukey post hoc analyses showed that per-ormance was identical in the masking tasks with a single target and

ith two targets presented in different hemifields (35% vs. 37%rrors, p � .9). Performance dropped significantly when two targetsere displayed in the same hemifield (by 12% compared with two

argets displayed in different hemifields p � .005), and by 11%compared with one single target, p � .01). These results suggest an

ffect of redundancy gain with targets presented in different hemi-elds.

In patients, performance also varied according to the task, butnly for some SOAs (Figure 5, right panel), as suggested by a signif-

cant interaction between type of task and SOA [F (10,170) � 3, p �.005, partial �2 � .15). Tukey post hoc analyses showed that perfor-

ance improved when two targets were presented in differentemifields compared with all other target conditions but only for

he SOA of 100 msec (by 20%, p � .005).

Figure 5. Comparison of correct response rates for pre-sentation of two targets (intrahemifield, empty circlesversus interhemifield, empty squares) versus one target(dotted curve with diamond) as a function of stimulusonset asynchronies (SOAs) in forward (SOAs � 0 msec)and backward (SOAs � 0 msec) masking condition.

www.sobp.org/journal

mpact of Treatment on PerformanceTo determine the impact of treatment on patients’ impairments

n masking tasks, we conducted the same ANOVA as describedarlier on correct responses in patients but with treatment in chlor-romazine equivalent as covariate. We found the same effects asescribed above.

iscussion

First, the results we obtained in our study reproduce deficits inasking tasks in schizophrenia patients already broadly described

n the literature (35,43– 45). With a single target, we found anmpairment in both backward and forward masking. Althoughome studies suggest a selective impairment in backward mask-ng, the results in the literature are mixed (46), and several stud-es have shown results close to ours (47). Most important, how-

Figure 4. Rate of correct responses when two squares arepresented in forward (stimulus onset asynchrony [SOAs] � 0msec) and backward (SOAs � 0 msec) masking condition.Patients’ (continuous line) and control subjects’ (dottedline) responses are represented on the left side for intra-hemifield presentation of the squares and on the rightside for interhemifield presentation.

aoSic

ttocawge(ipm

H(S

c

1

1

1

1

1

1

L. Lalanne et al. BIOL PSYCHIATRY 2012;71:162–168 167

ever, our results enabled us to explore both the advantage ofdetecting a single target compared with two targets, at least inbackward masking, as well as the advantage provided by theredundancy of signals across hemifields, especially in forwardmasking.

The most important result of this study is that the perfor-mance of patients and control subjects was similar in backwardmasking when there were two targets rather than one, but theydiffered in terms of their ability to benefit from focusing on asingle target. Control subjects’ performance improved with pre-sentation of one target compared with two. Patients’ perfor-mance, by contrast, either remained the same or improved lessthan that of control subjects. These results suggest that an im-pairment in terms of focused attention may account, at least inpart, for the masking deficits observed in patients. The resultscannot be explained in terms of a generalized deficit, whichwould have led to a larger impairment in the most difficultcondition, that is, with two targets. There are alternative expla-nations, however, in particular, the impact of redundancy, whichought to be considered first.

When presenting two targets instead of one, there is a redun-dancy gain. If patients benefit more than control subjects fromredundancy, this should be revealed when targets are displayedacross hemispheres because of interhemispheric transfer distur-bances (42). It would explain why performance of patients andcontrol subjects are equated when two targets are presentedacross hemifields. Disturbed attention focalization and enhancedredundancy both lead to a flattening of the performance differencebetween the conditions with a single target and with two targetspresented across hemifields. We bypassed this difficulty by compar-ing the presentation of two targets within and across hemifields. Asusceptibility to redundancy was expected to result in better per-formance for across- than for within-hemifield presentation, forboth backward and forward masking. This was not fully confirmed.Although patients improved for across- compared with within-hemifield presentation in backward masking, this was not statisti-cally larger in patients than in control subjects. Furthermore, inforward masking, performance improvement was somewhatsmaller in patients than control subjects, and better performancefor two targets displayed across rather than within hemifields wassignificant only for one SOA in patients. All in all, redundancy acrosshemifields might be an interesting avenue to explore but does notseem to explain fully why patients match control subjects’ perfor-mance in presentation of two targets rather than one. The lack ofadvantage provided by the presentation of a single target thereforehas more to do with altered attention focalization. It might besuggested that such alteration is related to impaired attentionalcapture in the single target presentation. Two targets are betterdetected because of the redundancy gain and thus might bettercapture attention. However, such a hypothesis would lead to thesame inconsistencies as the one related to the redundancy gain. Wethus propose that the patients’ impairment is related instead todifficulties in allocating attention to the target rather than the mask(33), that is, mechanisms requiring precise control of attention se-lection. These mechanisms have been suggested to be selectivelyimpaired in schizophrenia (34). Difficulties with allocating attention

ccurately in time and space may also account for the difficultiesbserved in patients in forward masking, two targets, and largeOAs. These conditions are characterized by the fact that present-

ng the mask first should help subjects to expect the target. This isertainly possible when the SOAs are large enough (48,49). This

hypothesis would be consistent with earlier results but requires

further study (33,50).

1

One of the limitations of our study is that most patients werereated, and an effect of treatment cannot be ruled out, although usinghe drug dosage as covariate did not change the results of the analysesf variance. Also, the similarity of the results obtained with patients andontrol subjects in the presentation of two targets seems to precluden explanation in terms of treatment. It should be confirmed, however,hether identical results would be found in a more symptomaticroup and whether the matching on education level led to an under-stimation of the impairment in patients relative to control subjects

51). However, our results do point to a possible impact of attentionmpairments in masking deficits in patients with schizophrenia. Ouraradigm might be of use in event-related potential studies to deter-ine for the effect of attention.

This research was financed by the French National Institute forealth and Medical Research, the University Hospital of Strasbourg

API-HUS n° 3494: Internal Project Grant from the University Hospital oftrasbourg), and the Medicine Faculty of Strasbourg.

The authors reported no biomedical financial interests or potentialonflicts of interest.

Supplementary material cited in this article is available online.

1. Cadenhead K, Serper Y, Braff DL (1998): Transient versus sustained visualchannels in the visual backward-masking deficits of schizophrenia pa-tients. Biol Psychiatry 43:132–138.

2. Green MF, Walker E (1986): Symptom correlates of vulnerability back-ward masking in schizophrenia. Am J Psychiatry 143:181–186.

3. Rund BR (1993): Backward-masking performance in chronic and non-chronic schizophrenics, affectively disturbed patients, and normal con-trol subjects. J Abnorm Psychol 102:74 – 81.

4. Saccuzzo DP, Braff DL (1981): Early information processing deficit inschizophrenia News findings using schizophrenic patients Centrally,not peripherally. Arch Gen Psychiatry 38:175–179.

5. Koelkebeck K, Ohrman P, Hetzel G, Arolt V, Suslow T (2005): Visualbackward masking: Deficits in locating targets are specific to schizo-phrenia and not related to intellectual decline. Schizophr Res 78:261–268.

6. Butler PD, Schechter L, Zemon V, Schwartz SG, Greenstein VC, Gordon J,et al. (2001): Dysfunction of early-stage visual processing in schizophre-nia. Am J Psychiatry 158:1126 –1133.

7. Tam WC, Liu Z (2004): Comparison of neurocognition between drug-free patients with schizophrenia and bipolar disorder. J Nerv Ment Dis192:464 – 470.

8. Green MF, Nuechterlein KH, Breitmeyer B, Mintz J (2006): Forward andbackward visual masking in unaffected siblings of schizophrenic pa-tients. Biol Psychiatry 59:446 – 451.

9. Lee J, Cohen MS, Engel SA, Glahn D, Nuechterlein KH, Wynn JK, et al.(2010): Regional brain activity during early visual perception in unaf-fected siblings of schizophrenia patients. Biol Psychiatry 68:78 – 85.

0. Sergi MJ, Rassovsky Y, Nuechterlein KH, Green MF (2006): Social percep-tion as a mediator of the influence of early visual processing on func-tional status in schizophrenia. Am J Psychiatry 163:448 – 454.

1. Breitmeyer B, Ögmen (2006): Visual Masking: Time Slices Through Con-scious and Unconscious Vision. Oxford, United Kingdom: Oxford Univer-sity Press.

2. Carter CS, Robertson LC, Chaderjian MR, Celaya LJ, Nordahl TE (1992):Attentional asymmetry in schizophrenia: Controlled and automatic pro-cesses. Biol Psychiatry 31:909 –918.

3. Van Assche M, Giersch A (2011): Visual organization processes in schizo-phrenia. Schizophr Bull 37:394 – 404.

4. Breitmeyer BG, Ganz L (1976): Implications of sustained and transientchannels for theories of visual pattern masking, saccadic suppression,and information processing. Psychol Rev 83:1–36.

5. Green M, Walker E (1984): Susceptibility to backward masking in schizo-phrenic patients with positive or negative symptoms. Am J Psychiatry141:1273–1275.

6. Keesey UT (1972): Flicker and pattern detection: A comparison ofthresholds. J Opt Soc Am 62:446 – 448.

www.sobp.org/journal

3

3

3

3

3

4

4

4

4

4

4

4

4

4

4

5

5

168 BIOL PSYCHIATRY 2012;71:162–168 L. Lalanne et al.

17. Kulikowski JJ, Tolhurst DJ (1973): Psychophysical evidence for sustainedand transient detectors in human vision. J Physiol 232:149 –162.

18. Tolhurst DJ (1973): Separate channels for the analysis of the shape andthe movement of moving visual stimulus. J Physiol 231:385– 402.

19. Schechter I, Butler PD, Silipo GVZ, Javitt DC (2003): Magnocellular andparvocellular contributions to backward masking dysfunction in schizo-phrenia. Schizophr Res 64:91–101.

20. Slaghuis WL (2004): Spatio-temporal luminance contrast sensitivity andvisual backward masking in schizophrenia. Exp Brain Res 156:196 –211.

21. Rassovsky Y, Green MF, Nuechterlein KH, Breitmeyer B, Mintz J (2004):Paracontrast and metacontrast in schizophrenia: Clarifying the mecha-nism for visual masking deficits. Schizophr Res 71:485– 492.

22. Di Lollo V, Enns JT, Rensink RA (2000): Competition for consciousnessamong visual events: The psychophysics of reentrant visual processes. JExp Psychol Hum Percept Perform 29:481–507.

23. Herzog MH, Kopmann S, Brand A (2004): Intact figure-ground segmen-tation in schizophrenia. Psychiatry Res 129:55– 63.

24. Del Cul A, Dehaene S, Reyes P, Bravo E, Slachevsky A (2009): Causal roleof prefrontal cortex in the threshold for access to consciousness. Brain132:2531–2540.

25. Dehaene S, Naccache L. (2001): Towards a cognitive neuroscience ofconsciousness: basic evidence and a workspace framework. Cognition79:1–37.

26. Ramachandran VS, Cobb S (1995): Visual attention modulates metacon-trast masking. Nature 373:66 – 68.

27. Tata MS (2002): Attend to it or lose it forever: Selective attention, meta-contrast masking, and object substitution. Percept Psychophys 64:1028 –1038.

28. Enns JT (2004): Object substitution and its relation to other forms ofvisual masking. Vision Res 44:1321–1331.

29. Carter CS, Robertson LC, Chaderjian MR, Celaya LJ, Nordahl TE (1992):Attentional asymmetry in schizophrenia: Controlled and automatic pro-cesses. Biol Psychiatry 31:909 –918.

30. Sereno AB, Holzman PS (1996): Spatial selective attention in schizophrenic,affective disorder, and normal subjects. Schizophr Res 20:33–50.

31. Spencer KM, Nestor PG, Valdman O, Niznikiewicz MA, Shenton ME,McCarley RW (2011): Enhanced facilitation of spatial attention in schizo-phrenia. Neuropsychology 25:76 – 85.

32. Giersch A, Rhein V (2008): Lack of flexibility in visual grouping in patientswith schizophrenia. J Abnorm Psychol 117:132–142.

33. Granholm E, Fish SC, Verney SP (2009): Pupillometric measures of atten-tional allocation to target and mask processing on the backward mask-ing task in schizophrenia. Psychophysiology 46:510 –520.

34. Luck SJ, Gold JM (2008): The construct of attention in schizophrenia. Biol

Psychiatry 64:34 –39.

www.sobp.org/journal

5. Rassovsky Y, Green MF, Nuechterlein KH, Breitmeyer B, Mintz J (2005):Modulation of attention during visual masking in schizophrenia. Am JPsychiatry 162:1533–1535.

6. Miller JO (1982): Divided attention: Evidence for coactivation with re-dundant signals. Cogn Psychol 14:247–279.

7. Mohr B, Pulvermüller F (2002): Redundancy gains and costs in cognitiveprocessing: effects of short stimulus onset asynchronies. J Exp PsycholLearn Mem Cogn 28: 1200 –1223.

8. Miller J (2004): Exaggerated redundancy gain in split brain: A hemi-spheric coactivation account. Cogn Psychol 49:118 –154.

9. Corballis MC (2002): Hemispheric interactions in simple reaction time.Neuropsychologia 40:423– 434.

0. Beaumont JG, Dimond S (1973): Brain disconnection and schizophrenia.Br J Psychiatry 123:661– 662.

1. Mohr B, Pulvermüller F, Cohen R, Rockstroh B (2000): Interhemisphericcooperation during word processing: Evidence for callosal transfer dys-function in schizophrenics patients, Schizophr Res 46:231–239.

2. Florio V, Marzi CA, Girelli, A, Savazzi S (2008): Enhanced redundancy gainin schizophrenics: a correlate of callosal dysfunction? Neuropsychologia46:2808 –2815.

3. Green MF, Nuechterlein KH, Mintz J (1994): Backward masking in schizo-phrenia and mania. II. Specifying the visual channels. Arch Gen Psychia-try 51:945–951.

4. Green MF, Nuechterlein KH, Breitmeyer B (2002): Development of acomputerized assessment for visual masking. Int J Methods Psychiatr Res11:83– 89.

5. Green MF, Nuechterlein KH, Breitmeyer B, Tsuang J, Mintz J (2003):Forward and backward visual masking in schizophrenia: Influence ofage. Psychol Med 33:887– 895.

6. Skottun BC, Skoyles JR (2009): Are masking abnormalities in schizophre-nia specific to type-B masking? World J Biol Psychiatry 10:798 – 808.

7. Green MF, Lee J, Wynn JK, Mathis KI (2011): Visual masking in schizo-phrenia: Overview and theoretical implications. Schizophr Bull 37:700 –708.

8. Nobre AC, Griffin IC, Rao A (2007): Spatial attention can bias search invisual short-term memory. Front Hum Neurosci 1:4.

9. Doherty JR, Rao A, Mesulam MM, Nobre AC (2005): Synergistic effect ofcombined temporal and spatial expectations on visual attention. J Neu-rosci 25:8259 – 8266.

0. Lalanne L, van Assche M, Giersch A (2010). When predictive mechanismsgo wrong: Disordered visual synchrony thresholds in schizophrenia[published online ahead of print September 27]. Schizophr Bull.

1. Miller GM, Chapman JP (2001): Misunderstanding analysis of covari-

ance. J Abnorm Psychol 110:40 – 48.