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Neuropsychologia 46 (2008) 1401–1414

Effects of emotional and non-emotional cues on visual search in neglectpatients: Evidence for distinct sources of attentional guidance

Nadia Lucas a,∗, Patrik Vuilleumier a,b

a Laboratory for Behavioural Neurology & Imaging of Cognition, Department of Neurosciences & Clinic of Neurology,University Medical Center, Geneva, Switzerland

b Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland

Received 3 April 2007; received in revised form 14 November 2007; accepted 19 December 2007Available online 6 January 2008

bstract

In normal observers, visual search is facilitated for targets with salient attributes. We compared how two different types of cue (expression andolour) may influence search for face targets, in healthy subjects (n = 27) and right brain-damaged patients with left spatial neglect (n = 13). Thearget faces were defined by their identity (singleton among a crowd of neutral faces) but could either be neutral (like other faces), or have a differentmotional expression (fearful or happy), or a different colour (red-tinted). Healthy subjects were the fastest for detecting the colour-cued targets,ut also showed a significant facilitation for emotionally cued targets, relative to neutral faces differing from other distracter faces by identity only.ealthy subjects were also faster overall for target faces located on the left, as compared to the right side of the display. In contrast, neglect patientsere slower to detect targets on the left (contralesional) relative to the right (ipsilesional) side. However, they showed the same pattern of cueing

ffects as healthy subjects on both sides of space; while their best performance was also found for faces cued by colour, they showed a significantdvantage for faces cued by expression, relative to the neutral condition. These results indicate that despite impaired attention towards the leftemispace, neglect patients may still show an intact influence of both low-level colour cues and emotional expression cues on attention, suggestinghat neural mechanisms responsible for these effects are partly separate from fronto-parietal brain systems controlling spatial attention during search.

2008 Elsevier Ltd. All rights reserved.

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eywords: Attention; Emotion; Spatial neglect; Visual search; Parietal; Orbitof

. Introduction

While our gaze is freely scanning the surrounding environ-ent, it may be caught by salient visual features that seemingly

op out of the background. Thus, on some occasions, our atten-ion might be involuntarily drawn to a smiling face, or andd-looking object, among a crowd of monotonous neutral stim-li. Likewise, in experimental situations, abundant research inormal subjects has shown that selective attention tends to bereferentially guided to salient or odd visual stimuli in a scene
Wolfe & Horowitz, 2004). Such effects have been observedot only for stimuli that differ from background items by aimple visual feature (e.g. colour or orientation), but also for
∗ Corresponding author at: Laboratory of Behavioural Neurology and Imag-ng of Cognition (LabNIC), Clinic of Neurology, University Hospital, 24 rue

icheli-du-Crest, 1211 Geneva 4, Switzerland. Tel.: +41 22 3728 478;ax: +41 22 3728 333.

E-mail address: [email protected] (N. Lucas).

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028-3932/$ – see front matter © 2008 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2007.12.027

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timuli with a particular emotional or social significance (Fox,usso, Bowles, & Dutton, 2001; Fox, Russo, & Georgiou, 2005;astwood, Smilek, & Merikle, 2003; Lundqvist & Ohman, 2005;illiams, Moss, Bradshaw, & Mattingley, 2005). For instance,

n visual search tasks, emotionally expressive face targets mayapture attention faster (Hahn, Carlson, Singer, & Gronlund,006; Ohman, Flykt, & Esteves, 2001) and/or more effec-ively (Eastwood et al., 2003; Fox et al., 2001, 2005; Fenske

Eastwood, 2003), as compared with neutral faces. Similarehavioural effects of emotional cues on spatial attention haveeen found in exogenous orienting tasks derived from Posneraradigm (e.g., Fox et al., 2001; Pourtois, Grandjean, Sander,

Vuilleumier, 2004). However, the nature of these emotionalnfluences on attention and visual search is still debated, asaces and expressions involve relatively high-level visual rep-
esentations that may not be extracted as efficiently as theore simple feature responsible for classic “pop-out” effects
Pessoa, Kastner, & Ungerleider, 2002; Wolfe & Horowitz,004).

mailto:[email protected]

dx.doi.org/10.1016/j.neuropsychologia.2007.12.027

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402 N. Lucas, P. Vuilleumier / Neur

At the neural level, recent brain imaging work in healthy sub-ects has begun to uncover the possible neural correlates for suchmotional facilitation of visual processing. Several studies havehown greater activation of extrastriate visual areas in responseo emotional stimuli (e.g. fearful faces), as compared to neutraltimuli (Ishai, Pessoa, Bikle, & Ungerleider, 2004; Vuilleumier,007; Vuilleumier, Armony, Driver, & Dolan, 2001). Emotionaltimuli also activate a network of specific limbic brain regions,uch as the amygdala, orbitofrontal cortex, anterior cingulate,nd insula (Haxby, Hoffman, & Gobbini, 2002). It has beenuggested that modulatory feedback from limbic regions (inarticular the amygdala) might act to increase activation ofisual areas (Amaral, Behniea, & Kelly, 2003; Vuilleumier,ichardson, Armony, Driver, & Dolan, 2004), and hence be

esponsible for preferential attention towards emotional visualtimuli (Vuilleumier, Armony et al., 2002; Vuilleumier, 2005).ccordingly, this emotional modulation might provide a sep-

rate top-down influence on visual processing that operatesn parallel, perhaps additively, to the top-down influencesxerted by classic attentional systems in fronto-parietal net-orks (Vuilleumier, 2005). Here we tested this hypothesis by

nvestigating whether emotional cues might still influence visualearch in patients with spatial neglect, who typically fail to directttention towards the contralesional side of space due to unilat-ral damage to the fronto-parietal attention systems (Driver &uilleumier, 2001; Milner & McIntosh, 2005; see also KastnerUngerleider, 2001).Spatial neglect is a frequent neurological syndrome, occur-

ing most often after right hemisphere lesions, particularly in thearietal or frontal lobe. It is characterized by abnormal biases andestrictions in spatial attention, leading to severe impairments inhe ability to perceive and/or explore stimuli on the side of spacepposite to the brain lesion (most often left space). Neglect isypically observed during visual search tasks, such as clinicalancellation tests (Gauthier, Dehaut, & Joanette, 1989) wherehe patients must mark all targets present in a visual array, butail to find those located on the contralesional half of the array,nd explore the ipsilesional half repeatedly instead (Mannant al., 2005). In these patients, the accuracy of stimuli in con-ralesional space is particularly slow, or even impossible, in theresence of competing distracters (Mark, Woods, Ball, Roth,

Mennemeier, 2004; Wojciulik, Rorden, Clarke, Husain, &river, 2004). This effect of competition is also illustrated by

he phenomenon of perceptual extinction on double stimula-ion, where a visual stimulus in the contralesional hemifield iserceived when presented alone, but not when presented withnother simultaneous stimulus in the ipsilesional field (Driver

Vuilleumier, 2001; Posner, Walker, Friedrich, & Rafal, 1987;afal, 1994). Thus, any competition for attentional resourcesill usually exacerbate the patients’ biases in attention or explo-

ation, and further reduce awareness of contralesional stimuli.Nevertheless, some categories of stimuli may compete more

fficiently for attention and seem more likely to reach awareness
hen presented in contralesional space, despite the pathologi-
al neglect biases of these patients. This modulation of attentionuggests that some residual processing may still take placeithout attention and subsequently guide attention towards

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hologia 46 (2008) 1401–1414

hese stimuli (Berti, 2002; Driver & Vuilleumier, 2001). Fornstance, in patients with visual extinction, faces with angryr happy expressions are more frequently detected than neu-ral faces in the contralesional field (Fox, 2002; Vuilleumier

Schwartz, 2001b). Similarly, bodies with emotional gesturesre less extinguished than neutral bodies (de Gelder, 2006); andictures of spiders are less extinguished than pictures of flowersVuilleumier & Schwartz, 2001a). Altogether, these results con-erge with the findings in healthy subjects that emotional stimuli,ncluding facial expressions, may effectively attract attentionnder conditions of competition with neutral stimuli (Eastwoodt al., 2003; Fox et al., 2001). However, to our knowledge, notudy has investigated whether such effects of affective facialxpression might also bias attention in a visual search taskn neglect patients. The fact that emotional cues might allevi-te visual extinction in some cases (Fox, 2002; Vuilleumier &chwartz, 2001a, 2001b) does not necessarily predict that sim-

lar effects might arise in a visual search task, because searchnvolves some exploratory components that do not contributeo perceptual performance during extinction tests, implies moreerial processes in the deployment of attention, and typicallyntails a much greater load by concomitant distracters (seeusain & Kennard, 1997; Rapcsak, Verfaellie, Fleet, & Heilman,989). Moreover, deficits in cancellation tasks and perceptualxtinction may dissociate in some patients with neglect (Azouvit al., 2002; Cocchini, Cubelli, Della Sala, & Beschin, 1999;imm et al., 2001; Stone, Halligan, Marshall, & Greenwood,998), suggesting that these manifestations have partly differenteural substrates (see Karnath, Himmelbach, & Kuker, 2003).

Several studies have previously investigated visual search foreutral targets in neglect, usually to compare parallel/feature anderial/conjunction searches, with a variety of different stimulind different paradigms (for overview, see Behrmann, Ebert,

Black, 2004). The results have often remained inconclu-ive. Some studies found evidence for intact feature searchn contralesional space (i.e. with intact “pop-out” effects foreature singletons regardless of the number of distracters), sug-esting that early “pre-attentive” visual mechanisms extractinghese visual features may still operate normally in patientsith spatial neglect (Aglioti, Smania, Barbieri, & Corbetta,997; Esterman, McGlinchey-Berroth, & Milberg, 2000). Othertudies found that search for targets defined by a single fea-ure (e.g., colour, possibly involving parallel “pre-attentive”rocesses) and search for targets defined by a conjunction ofeatures (e.g., colour + shape, presumably requiring serial atten-ive processes) both were disrupted in neglect patients (seeehrmann, Ebert et al., 2004; Pavlovskaya, Ring, Groswasser,Hochstein, 2002; Riddoch & Humphreys, 1987). The latter

ndings suggest that damage to attentional systems in fronto-arietal networks may impair visual exploration and detectionf salient visual attributes in contralesional space during searchasks, even though such attributes may be processed at somere-attentive stages and produce implicit effects in other tasks
see Berti, 2002). Because faces and expressions are complexisual stimuli defined by specific features as well as a conjunc-ion of features (Maurer, Grand, & Mondloch, 2002; Suzuki
Cavanagh, 1995), and yet may be processed to some extent

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N. Lucas, P. Vuilleumier / Neur

ithout attention (Mack & Rock, 1998; Ro, Russell, & Lavie,001; Vuilleumier, Sagiv et al., 2001) and even without con-cious awareness (de Gelder, Vroomen, Pourtois, & Weiskrantz,999; Morris, DeGelder, Weiskrantz, & Dolan, 2001; Pegna,hateb, Lazeyras, & Seghier, 2005), it is unclear whether search

or emotional faces would be more or less preserved than sim-le feature search in patients with spatial neglect. Our presentoal was therefore to test how emotional information modu-ates the “threshold” for attention and awareness (Duncan &arrett, 2007; Gaillard et al., 2006)—rather than to manipu-

ate awareness to examine effects on processing of emotionalnformation.

In our study, we asked firstly whether visual search woulde guided more efficiently to emotional vs. neutral faces ineglect patients, as previously found in normal subjects (e.g.astwood et al., 2003; Fox et al., 2001), despite impaired atten-

ion towards contralesional space. Secondly, we also askedhether any deficit in search would dissociate between emo-

ional and simple/low-level feature (colour) cues. Thirdly, wexamined whether any emotional advantage during search foraces might differ between negative and positive expressionsi.e., fearful and happy). We designed a simple visual searcharadigm in which patients had to report the gender of a targetace, whose identity was unique amongst an array of distractersith a different identity. Distracter faces were always neutral.ritically, the target face could differ from the distracters by

dentity alone (neutral baseline), by identity plus expressionfearful or happy), or by identity plus colour (red hue).

Besides longer latencies for detecting target faces in contrale-ional/left space, as expected in neglect patients, we predictedwo possible outcomes of major theoretical importance: Ifome “pre-attentive” processing of emotional expression (and/orolour singleton) is intact in neglect patients, and separate fromhe serial attention processes mediated by fronto-parietal sys-ems, then target faces cued by a different expression (or aifferent colour) should yield a similar facilitation on both sidesf space, with a purely additive gain of these cues over and aboveny abnormal spatial biases in search (but with no interaction).n the contrary, if visual processes favouring the accuracy of

motional faces (and/or colour singleton) depend on the samettentional systems in fronto-parietal areas that are damaged ineglect patients, then any facilitation for emotional faces (orolour singleton) should be lost in contralesional space, or inter-ct with the pathological disruption of search on that side. Ouresults support the first hypothesis, by showing that emotionalnfluences on visual search are independent from (but addi-ive to) the mechanisms of spatial attention that are affected byeglect.

. Methods

.1. Participants

All subjects, healthy and brain-damaged, consented to participate in thistudy after giving their informed consent according to the local ethics. Healthyarticipants were 27 volunteers recruited via advertisement at Geneva Universitynd University Hospital. They included 12 males and 15 females, all right-anded (except one left-handed), with a wide age range in order to provide

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hologia 46 (2008) 1401–1414 1403

ppropriate controls for the patients (range = 22–94, average = 42.9), and hado history of neurological or psychiatric illness. All subjects had normal ororrected-to-normal view.

The patient group consisted of 13 subjects (4 male, 9 female) who sufferedrom spatial neglect after right unilateral first-ever stroke. They were recruitedrom a consecutive series of patients admitted to the Neurology Department ateneva University Hospital. All patients met the following criteria: they were

ight-handed; aged 39.6–83.7 years (mean age 67.6 years); with clinical andadiological evidence of a single, focal lesion of the right hemisphere due totroke, involving the middle cerebral artery (MCA) territory; with no other seri-us concomitant illness. They were examined 15 days post-stroke on average,nd included only if they could participate in our computerized search task (i.e.ith stable vigilance, sufficient cooperation, and no discouraging fatigue during∼30 min exam). Neglect was assessed with a standard battery of tests (Azouvit al., 2002; Rousseaux et al., 2001), including cancellation, line bisection, andrawing. To quantify the severity of neglect symptoms, we calculated a com-osite score, based on the number of tests showing significant impairments, asommonly used in clinical research (e.g. Azouvi et al., 2002; Wilson, Cockburn,

Halligan, 1987). Patients showing neglect on all three categories of tests (can-ellation, bisection, drawing) were classified as “severe”; whereas those showingeglect on one or two of these tests were classified as “mild” (see Table 1b).lthough somewhat arbitrary, this global composite score provided a simple and

easonable index for the severity of attentional disturbances, despite the possi-le heterogeneity of the neglect syndrome (e.g. see Karnath, Fruhmann Berger,uker, & Rorden, 2004). For further patient details, see Tables 1a and 1b.

.2. Material and procedure

Patients were tested on a portable HP computer with a 15.4 inch wide monitorresolution 1680 × 1050), positioned on a table ∼50 cm in front of them, in auiet dimly lit room. The E-Prime Software (Version 1.1.4.1) was used fortimulus presentation and response collection.

Our visual stimuli were photographs of faces selected from the Karolinskairected Emotional Faces dataset (KDEF; Lundqvist, Flykt, & Ohman, 1998).e used 16 different face identities (8 women and 8 men), which could serve

ither as targets or distracters in different trials. Each individual face could haveither a neutral, happy, or fearful expression. All these photographs were inreyscale; but in addition we created an extra colour version of each neutral face,y increasing red hue saturation in the picture, such that the face appeared slightlyed-tinted. Note that this colour difference was relatively subtle, in order to avoidaking these pictures conspicuously different from all others (see Fig. 1). Thus,

n total, we had four different versions for each face stimulus: neutral, happy,earful, or red-coloured.

Each trial started with a white central fixation cross on black background,hown for 800 ms. Next followed a search array, where 8 faces were arranged incircle around a central fixation cross (Fig. 1). The faces always included sevenistracters (all with the same identity and a neutral expression), plus anotheringle face that was the target and had a different identity (face singleton). Crit-cally, this target face could differ from the other seven distracter faces by eitherdentity alone (ID-only condition), identity + expression (either fear: ID + FEARondition; or happy: ID + HAP condition), or identity + colour (ID + COL con-ition). The target could occupy any of the eight possible positions in the arraynd was unpredictable. Target type and position were randomly varied acrossuccessive trials, with an equal probability of all positions for the different tar-et types. Participants were asked to detect the face singleton among the crowdf the seven similar distracters, and to report its gender (male vs. female), asuickly as possible. Responses were made on two arrow keys on the computerey-pad, with all other keys being inactivated. The face array remained on thecreen till a response key was pushed, or up to a maximum time-limit (15 s inealthy subjects, 35 s in patients). After an inter-trial interval of 1500 ms, theext trial started. If the subject did not respond within the time-limit, a warningignal appeared (for 1500 ms) and encouraged the subject to speed up in the nextrial.

Each subject participated in the search task in 2 blocks of 64 randomlyntermixed trials, with the different blocks including different combinations ofaces arranged in a pseudorandom manner. A brief training block with a differentet of faces was always given first in order to familiarize participants with theask.

1404 N. Lucas, P. Vuilleumier / Neuropsychologia 46 (2008) 1401–1414

Table 1aDemographic and clinical patient data

Patient Sex Age Cerebral vascularaccident

Arterial territory Days post-accident Handedness VF loss Left visualextinction

Neglectseverity

MM f 39.69 i MCA 8 r No Yes +SC f 59.59 h MCA 16 r No No +MC f 75.76 i MCA 15 r No No ++PG f 75.12 i MCA 4 r No No ++ST f 77.95 i MCA 80 r No No ++AJ m 54.96 h MCA PCA 12 r Yes Yes +++CC f 60.48 i MCA;ACA 11 r No No +++FR m 76.46 i MCA 5 r No No +++FA f 67.66 i MCA 12 r No Yes +++GR m 57.74 h MCA 13 r Yes Yes +++MB f 79.31 i MCA 5 r Yes No +++ME f 77.79 i MCA 9 r No Yes +++RP m 60.20 i MCA 13 r No No +++

f: female; m: male; i: ischemic; h: hemorragic; MCA: middle cerebral artery; PCA: posterior cerebral artery; ACA: anterior cerebral artery; r: right; +: neglectsymptoms on 1/3 tasks; ++: neglect symptoms on 2/3 tasks; +++: neglect symptoms on 3/3 tasks.

Table 1bPatients’ performance on neglect tests

Patients Neglectseverity

Bells cancellation test Line bisectiondeviation (mm)

Drawing Left visualextinction

Difference between leftvs. right side omissions

First bellcancelled

MM + 3 7 3.1 5 YesSC + 4 7 4.5 5 NoMC ++ −1 7 8 5 NoPG ++ 3 5 2 4 NoST ++ 14 7 12 5 NoAJ +++ 9 7 10 2.5 YesCC +++ 9 7 17.6 5 NoFR +++ 13 7 39.3 1 NoFA +++ 7 7 8 4 YesGR +++ 13 7 11 1.5 YesMB +++ 10 5 39 1.5 NoME +++ 5 7 10 5 YesRP +++ 4 7 11.8 2 No

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eglect severity was based on the number of tests showing significant impairmeight side omissions (>2 = pathological); position of first bell cancelled from lefines (>6.5 mm = pathological). Drawing: copy of Gainotti scene (maximum 5 f

Note that we did not manipulate set size (number of distracters) in ouraradigm, as frequently done in studies of visual search in normal observers.
ndeed, our aim was not to obtain a precise measure of search slopes (latencyor cue × number of distracter), but rather to test for the effect of different facialues on spatial biases in search in neglect patients (latency for cue × side of thearget), while collecting sufficient trials per condition in this relatively difficult
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ig. 1. Visual search task: illustration of the four different conditions. The target facey identity + happy facial expression, identity + fearful facial expression, or by identach of the eight positions. (For interpretation of the references to colour in this figur

ng the three following tasks. Bells cancellation test: difference between left vs.t (1) to rightmost (7) (>5 = pathological). Line Bisection: deviation on 200 mmelements copied).

ask for the patients. Moreover, previous studies in healthy subjects have alreadyhown that emotional effects on visual search do not depend on specific set size
ange (Eastwood et al., 2003; Ohman & Soares, 1998). As neglect patientsypically show an asymmetry in search times, at the expense of targets on theontralesional as compared to the ipsilesional side of space, we relied on thisactor to probe for the same theoretical issue as set-size, that is, whether facial
could differ from the distracters (all with same identity) either by identity alone,ity + red hue. The probability of each target type was randomly distributed fore legend, the reader is referred to the web version of the article.)

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sinTtp < .0001; and ID + HAP: 1649.4 ms, t(26) = 3.46, p < .005).Importantly, healthy subjects detected the emotional target facessignificantly faster than neutral faces (ID-only vs. ID + FEAR:t(26) = 4.60, p < .0001; ID-only vs. ID + HAP: t(26) = 3.94,


motion produced additive or interactive effects on the asymmetrical distributionf attention (and search times) in patients.

Note also that the face dataset was carefully designed to normalize all itemsn terms of luminance, size, and feature position (eye-mouth) across picturesLundqvist et al., 1998), allowing us to estimate the inter-stimulus varianceetween images in different conditions. We calculated the amount of low-levelictorial similarity between different types of faces, using pixelwise correla-ion methods (as employed by others, see Bentin et al., 2007; Thierry, Martin,owning, & Pegna, 2007; see also Vuilleumier, Henson, Driver, & Dolan, 2002).his analysis provided a quantitative estimate of the interstimulus perceptualariance (ISPV) by comparing the image overlap on a pixel-by-pixel basis,sing normalized luminance values, for all possible pairs of items in differenttimulus conditions (Thierry et al., 2007). Although this index may not perfectlyapture information that is subjectively most salient in object recognition, ourse for faces with normalized size and feature position ensured a reliable andbjective measure of physical resemblance between conditions that may influ-nce visual search efficiency (Wolfe & Horowitz, 2004). This analysis indicatedreater pictorial similarity between different expressions of the faces (r = 0.86)han between different genders (r = 0.66, t = 4.67, p < .001) or between differentdentities (r = 0.54, t = 14.85, p < .001), suggesting that any low-level differencesue to emotional facial expression were minor as compared with the variationngendered by either gender or identity differences. Because search efficiency isritically dependent on the similarity of distinctive features between targets andistracters (Wolfe & Horowitz, 2004), any advantage of emotional cues couldherefore not be explained by systematic low-level stimulus features (i.e. greaterisual dissimilarity).

.3. Data analysis

Two dependent variables, reaction times (RT) and accuracy rates (AR) werenalysed. Accuracy was calculated as the percentage of target correctly recog-ized (correct gender reported for the target face) within the given time-limit,or each target type and each side of the array (four positions on the right andour positions on the left), for each participant. This procedure allowed us toefine targets based on facial features unrelated to expression and to maximizehe number of useful “target present” trials (no “absent target” trial) withoutxcessive task duration in the patients. Note that two types of error were there-ore possible (incorrect gender or misses), but not considered separately becausehey showed similar patterns across conditions (in both normals and patients).

oreover, because target and distracter faces were counterbalanced for genderequal number of trials where target and distracters were of the same gender, oronversely, of the opposite gender), we could verify that there was no system-tic response biases in reporting gender from the distracter faces vs. target facesee Section 3). Median RTs were calculated using correct trials only, for eachondition (four target types × two sides) and each participant.

For both subject groups (patients and normals), these data were then submit-ed to repeated measure ANOVAs using the within-subject factors of TARGETIDE (2) [contralesional (left); ipsilesional (right)], and CUE CONDITION (4)ID–only; ID + FEAR; ID + HAP; ID + COL]. In addition we also tested for theetween-subject factors of AGE (2) [<50 years, n = 20; vs. >50 years, n = 7] in theontrol group, as well as NEGLECT SEVERITY (2) [high vs. low] and VISUALIELD DEFECT (2) [present, not present] in the patient group. Post-hoc andlanned comparisons were performed using t-test.

.4. Lesion site analysis

Brain lesions were confirmed by clinical MRI scans in 12 patients and recon-tructed on axial slices using MRIcro, Version 1.39 (Rorden & Brett, 2000),ollowing previously described methods (Karnath et al., 2004; Mort et al., 2003;uilleumier et al., 2007). In one patient, we used CT scan to delineate the lesion

ite on a corresponding MRI template, as MRI could not be performed for clini-al reasons. The lesioned areas were then transformed to a 3D region-of-interest
ROI) corresponding to the lesion volume, and normalized to a standard brainemplate using standard MRIcro and SPM methods (Ashburner & Friston, 1997;shburner, Neelin, Collins, Evans, & Friston, 1997). The normalized lesion ROIsere superimposed on a T1 MRI template and submitted to exploratory mapping
nalyses using MRIcro (Rorden & Brett, 2000) methods, in order to examine the

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hologia 46 (2008) 1401–1414 1405

orrelations between behavioural performance and anatomical extent of brainamage on a voxel-by-voxel basis. Thus, we determined the average lesion over-ap across all neglect patients. In addition, we assessed critical lesion sites as

function of specific behavioural deficits in individual patients (e.g., neglecteverity), or as a function of their sensitivity to emotional cues in the visualearch task (see main text below).

. Results

We first describe the performance of healthy subjects, forubsequent comparison and interpretation of the results obtainedn neglect patients. For each group, we analysed both accuracyates and latencies of correct responses to the target face, forach of the four critical target conditions.

.1. Healthy subjects

.1.1. RT analysisLatencies to detect the face singleton was strongly influ-

nced by the cueing conditions. The 2 × 4 ANOVA of correctTs with the factors of TARGET SIDE and CUE CONDI-ION revealed two significant main effects, but no significant

nteraction. Healthy subjects were much faster to report botholour-cued and emotionally-cued faces, relative to the neutralace targets (Fig. 2), as indicated by the highly significant mainffect of CUE CONDITION (F(3,24) = 30.917; p < .0001). Inddition, healthy subjects were also generally faster to detectarget faces on the left side of the display, relative to the rightide (mean of median RTs, left, 1658.94 ms vs. right, 1706.5 ms;(1,26) = 7.132; p < .050). The effect of different cueing con-itions was however not different for targets on the right asompared to the left side, as confirmed by the lack of interactionetween these two factors (F(3,24) = 1.798; p > .05).

Pairwise comparisons between each CUE CONDITIONhowed that RTs were the fastest for “pop-out” red target facesn the ID + COL condition (1370.3 ms), as compared with theeutral condition (ID-only: 2022.2 ms, t(26) = 12.11, p < .0001).hese colour targets were also significantly faster than the

wo emotional conditions (ID + FEAR: 1699.2 ms, t(26) = 5.78;

ig. 2. Visual search task performance: results in healthy subjects (n = 27).ean response latencies and standard errors are plotted for the four face target

onditions.

1406 N. Lucas, P. Vuilleumier / Neuropsychologia 46 (2008) 1401–1414

Table 2Accuracy rate (% correct) for healthy subjects and neglect patients

Group Target side Condition

ID + FEAR ID + HAPPY ID-only ID + COLOUR

Mean S.D. Mean S.D. Mean S.D. Mean S.D.

Controls > 50years

Left 94.35 8.90 99.11 2.36 98.51 2.61 100.00 0.00Right 100.00 0.00 99.11 2.36 97.92 2.69 99.11 2.36

Controls < 50years

Left 96.98 3.73 95.94 7.10 95.94 5.83 97.81 3.67Right 96.88 4.76 95.94 5.83 93.54 7.18 97.19 4.29

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patients are shown in Fig. 3. Patients were slower to detectthe target face singletons on the left side of the display,as expected, but they were nevertheless influenced by thedifferent cueing conditions. Their RT data were first anal-

eglectatients

Contralesional 93.72 6.25 93.27Ipsilesional 92.28 6.32 94.09

< .001). There was no significant difference between fearfulnd happy faces (ID + FEAR vs. ID + HAP: t(26) = 1.69, p > .05).

Further planned comparisons for targets on the left andight side, considered separately, showed the same patternn both sides of the visual array (all comparisons betweenue conditions as above, p > .05), with no significant effectf target side when comparing right vs. left targets in eachcondition.

.1.2. Accuracy analysisPerformance of the healthy subjects was generally good

n all conditions (mean 97.1% correct; see Table 2). A 2 × 4NOVA on accuracy rates (AR) with the factors of TAR-ET SIDE and CUE CONDITION showed no significantifference as a function of side (mean correct for left tar-ets = 97.01%; right targets = 96.70%; F(1,26) = 0.22); whilehere was a tendency for less accurate detection of target facesn the ID-only condition (95.64%) relative to the other cue con-itions (ID + COL: 98.03%; ID + FEAR: 96.99%; ID + HAP:6.76%; F(3,24) = 2.79, p = .06). There was no significantnteraction between TARGET SIDE and CUE CONDITIONF(3,24) = 0.859).

.1.3. Age-related effectsGiven that stroke patients are generally older, we verified

hat search performance would not be affected by age differ-nces. To constitute a control group age-matched with patients,e split the 27 healthy participants into those above 50 yearsld (range = 55–94, mean = 76.14, n = 7) or below 50 yearsld (range = 22–39, mean = 28.35, n = 20). Note that mean agef the elderly group was comparable to the neglect patientsmean = 66.7). We then performed a 2 × 2 × 4 ANOVA on RTsith AGE GROUP as a between-subject factor, in addition to

he within-subject factors of TARGET SIDE and CUE CON-ITION as above. Not surprisingly, there was a significantain effect of AGE (F(1,25) = 37.7, p < .001) due to general

lowing in the elderly (mean RTs: 2690.5 ms) relative to theounger group (mean RTs: 1330.1 ms), but the main effects ofUE CONDITION (F(3,23) = 33.20, p < .0001) and TARGET
IDE (F(1,25) = 7.30, p < .01) remained unchanged. Impor-
antly, the pattern of cueing effects was similar for both ageroups. Although there was a significant interaction of CUEONDITION × AGE GROUP (F(3,23) = 3.87, p = .037), this

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7.42 85.92 10.86 91.35 11.288.77 85.42 15.20 97.12 5.48

as due to a greater magnitude of facilitation in elderly thanounger subjects for all cueing conditions, relative to the neu-ral face targets (mean RT differences = 708.5 vs. 357.78 ms).owever, a direct comparison of these RT differences (ID-nly minus ID + COL or ID + FEAR or ID + HAP) showed mainffects of age group (F(1,25) = 6.64, p < .01) and cue conditionF(3,23) = 14.07, p < .001) but no interaction between age andue condition (F(3,23) = 1.33). Moreover, when repeating anal-ses on RTs for each age group separately, the same pattern offfects was found for all cueing conditions as described aboveor the whole population.

There was also a slightly higher accuracy in elderly rela-ive to younger subjects (mean correct = 98.51% vs. 96.28%,(1,25) = 54.44, p = .028) but no interaction of age with anyther factors for target detection rates. Thus, overall, the effectsf colour and emotional cues on face search times were notodified by age, and still significant in the elderly control group

mean age = 76.1 years). Moreover, the preserved pattern foundn patients (see below) also confirmed that cueing effects onisual search were not influenced by age.

.2. Neglect patients

.2.1. RT analysisResponse latencies for correct target detection in neglect

ig. 3. Visual search task performance: results in neglect patients (n = 13). Meanesponse latencies and standard errors are plotted for the four face target condi-ions.

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sed using a repeated-measure ANOVA with the factors ofARGET SIDE (2) and CONDITION (4), as for healthyubjects above. The results revealed a main effect for TAR-ET SIDE (F(1,12) = 6.936; p < .05): neglect patients showed

onger latencies to detect contralesional/left-side targets (meanT = 4936.94 ms) as compared with ipsilesional/right-side tar-ets (mean RT = 4480.08 ms). This asymmetry was thus oppositeo the left advantage shown by normal subjects, and consis-ent with left spatial inattention. More important, the mainffect of CUE CONDITION was also highly significantF(3,10) = 7.91; p < .005), and crucially did not interact withARGET SIDE (F(3,10) = 0.35; p > .05). This indicates that theueing effects that preferentially guide attention to the morealient target faces were similarly expressed on both sides ofpace.

Further detailed analyses confirmed that the pattern of cueingffects between the different target conditions was symmetricaln both sides of the display in these patients, and similar to thatbserved in healthy subjects. Thus, correct response latenciesere the fastest for “pop-out” targets differing from distractersy ID + COL (mean RT = 4021.14 ms); followed by latenciesor emotional targets, which differed from distracters by eitherD + HAP expression (mean RT = 4550.85 ms) or ID + FEARxpression (mean RT = 4577.77 ms); while response latenciesere the longest for neutral targets that differed from distracter

aces by ID-only (mean RT = 5684.29 ms). Paired compar-sons also confirmed significant differences between emotionalnd neutral targets (ID + FEAR vs. ID-only: t(12) = 3.14,< .01; ID + HAP vs. ID-only: t(12) = 2.53, p < .05), as wells between colour and neutral targets (t(12) = 3.44, p < .005);hereas the difference between colour and emotional cuesas marginal (ID + FEAR vs. ID + COL: t(12) = 1.85, p = .09;

D + HAP vs. ID + COL: t(12) = 2.03, p = .065). This patternherefore clearly indicates that both colour and emotionalueing could still operate for targets on either side ofhe display, over and above the spatial bias due to lefteglect.

Even though the interaction between TARGET SIDE andUE CONDITION was not significant, we performed furtherlanned comparisons to confirm directly that the facilitationf target detection by the different cue conditions was presentn each side of space. When comparing latencies for contrale-ional targets only, using a repeated-measure ANOVA with theactor CUE CONDITION, we still found a highly significantffect (F(3,9) = 7.62; p < .005). Pairwise comparisons betweenhe four different cueing conditions also revealed significantlyonger latencies for ID-only relative to each of the other three cueonditions (ID + COL: p < .01; ID + HAP: p < .05; ID + FEAR:< .05). Similar results were found when comparing latencies

or ipsilesional targets only. Not only was there a main effect ofUE CONDITION (F(3,9) = 4.52; p < .05), but pairwise com-arisons showed significantly longer latencies for targets in theD-only condition (mean RT = 5400.69 ms) as compared with
he ID + COL (mean RT = 3822.04 ms; p < .01) and ID + FEARmean RT = 4260.92 ms; p < .05) conditions, and a marginal dif-erence with the ID + HAP condition (mean RT = 4436.65 ms;< .09).
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hologia 46 (2008) 1401–1414 1407

.2.2. Accuracy analysisCorrect detection rates in the patients indicated a similar pat-

ern of cueing effect on search performance as their RT data.repeated-measure ANOVA with the factors TARGET SIDE

2) × CUE CONDITION (4) showed a significant main effectf the factor CUE CONDITION (F(3,10) = 9.3, p < .001), but noffect of TARGET SIDE (F(1,12) = 0.37), and no interaction.atients were most accurate for detecting the face targets in theD + COL condition (94.23% correct), followed by ID + HAP93.68%) and ID + FEAR (93.00%), while they were worse inhe ID-only condition (85.67%).

Again, planned comparisons between cue conditions for leftnd right targets separately showed the same (significant) dif-erences for colour-cued and emotionally cued faces relativeo neutral faces on both sides (see Table 2). Neglect patientsetected contralesional face targets significantly less in theD-only condition (mean correct = 85.92%) as compared withD + COL (mean accuracy = 91.35%; p < .05), ID + FEAR (meanorrect = 93.72%; p < .05), and ID + HAP conditions (93.27%;< .01).

Likewise, for ipsilesional face targets, detection accuracy washe worst in the ID-only condition (85.42%), relative to all threether cue conditions (ID + COL: p < .005; ID + HAP: p < .05;D + FEAR: p < .05). Here again, these data indicate that patientsith spatial neglect took significant advantage of both types of

ues, emotional facial expression and colour pop-out.

.3. Check for response biases

Because distracter faces had the same gender as the targetace on half of the trials, correct responses might at least in prin-iple be made occasionally by naming the gender of distracters,ather than the target, or simply by chance. However, target andistracter faces were counterbalanced for gender (equal numberf female targets among female or male distracters, and viceersa, in randomised order). Therefore, if correct answers wereiven by chance or based on other faces, we would expect anqual number of incorrect gender responses to same-gender tar-ets (e.g. reporting male or female for a male among other maleaces) and to different-gender targets (e.g. reporting male oremale for a male among female faces). If so, we would thenave found an accuracy of “correct” answers of at most 50%in all or most conditions), that is, at chance level. However, thisas definitely not the case: mean accuracy was 96,8% in healthy

ubjects, and 92% in neglect patients (see Table 2). Moreover,here was no significant difference between conditions whenarget and distracters had either the same or different gender. Ineglect patients, gender was correctly reported on 94% for tar-ets among faces of the same gender and 89% for targets amongaces of different gender (while mean RTs were slower in theormer than the latter case: 5514 ms vs. 4452 ms, consistent withreater similarity and hence longer search times).

Furthermore, and most importantly, we found a similar
attern of emotional cueing effects on RTs for these twoonditions (same-gender vs. different-gender targets). Whenepeating ANOVA on correct RTs with the additional factorf Target Gender (same vs. different as distracters), in neglect

1 opsychologia 46 (2008) 1401–1414

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Table 3Relative advantage in search for cued, as compared to uncued faces

Group Target side Index

(N − F)/N (N − H)/N (N − R)/N

Neglect patientsContralesional 0.1564 0.1941 0.2876Ipsilesional 0.1457 0.1144 0.2858

Controls > 50 yearsLeft 0.1605 0.1764 0.2399Right 0.1470 0.2174 0.2803

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atients, we found an interaction only with the factor Targetide (F(1,12) = 6.015; p < .05), indicating greater slowing byender similarity on the contralesional side (mean RT for sames. different gender: 5966 ms vs. 4607 ms) as compared withhe ipsilesional side (mean RT for same vs. different gender:061 ms vs. 4297 ms). Most notably, the factor Target Gender didot interact with Cueing Condition (F(3,10) = 0.655; p > .05),nd the triple interaction Target Gender × Target Side × Cueingondition did not show any effect (F(3,10) = 0.471; p > .05).hus, both accuracy and RT data did not support the presencef any response bias in either group.

.4. Effects of neglect severity

In complementary analyses, we asked whether the cueingffects observed might be modulated by the severity of neglect,nd become reduced for left-side targets when spatial biasesowards the ipsilesional side increase. To examine this question,e separated our patients into two subgroups based on the sever-

ty of their neglect signs. Neglect severity was determined by theerformance on standardised clinical tests (bell cancellation, lineisection, drawing; Rousseaux et al., 2001). We distinguishedetween patients with marked symptoms, who showed neglectn all three of these tests; and patients with mild symptoms whohowed neglect on one or two of these tests only (see Table 1). Wehen analysed RTs and DRs in the face search task using three-ay ANOVAs with TARGET SIDE (2) and CUE CONDITION

4) as within-subject factors, and NEGLECT SEVERITY (2) asbetween-subject factor.

For the latency measures, results again showed a significantain effects of CUE CONDITION (F(3,9) = 7.55; p < .005),

ut no interaction of this factor with NEGLECT SEVERITYF(3,9) = 0.35), and no triple interaction (F(3,9) = 0.297). A sim-lar result was found for accuracy: the main effect of CUEONDITION was significant (F(3,9) = 8.381; p < .005) but didot interact with NEGLECT SEVERITY (F(3,9) = 0.73), andhere was no triple interaction (F(3,9) = 0.573).

.5. Cue facilitation effects: comparison healthyubjects—neglect patients

To further assess whether the cueing effects found in neglectatients were relatively intact, and proportionally similar tohat observed in healthy subjects despite overall slowing inhe patients, we also computed a ratio of the RT facilitationn the three cue conditions (colour, fear, happy) as comparedo the neutral condition, divided by RTs in the neutral condi-ion ([RTID-only − RTcue]/RTID-only), for each of the participantn each group. This ratio provides a direct measure of the rela-ive advantage in search for the cued faces, as compared with thencued faces. Comparing these ratios between the healthy andatient groups (Table 3) revealed no significant differences forach cue-type and each target side. A mixed 2 × 3 × 2 ANOVA
n these ratios with the within-subject factors TARGET SIDEnd the three CUE CONDITION, plus the between-subjectactor GROUP (healthy subjects vs. neglect patients), showed
significant effect of CUE CONDITION (F(2,37) = 48.758;

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< .0001), but no interaction of this factor with neither GROUPF(2,37) = 3.193; p > .05) nor TARGET SIDE (F(2,37) = 0.288;> .05); and no triple interaction (F(2,37) = 1.451; p > .05).hus, patients with spatial neglect apparently took the same

elative benefits from both kinds of cues as healthy subjects.

.6. Lesion site analysis

Finally, we performed a subsidiary analysis of the patients’esions to explore any possible relationship between the extentf brain damage and behavioural performance. This exploratorynatomical analysis must be taken with relative caution, how-ver, because our sample is relatively small for strong inferencesbout differential lesion patterns in relation to clinical symptomse.g. see Karnath et al., 2004). Lesion ROIs were defined on braincans for each patient (see Section 2) and then analysed using

RIcro (Rorden & Brett, 2000).First, we determined the average lesion sites in our patient

roup by plotting the common overlap of all 13 patients with spa-ial neglect, on a standard brain anatomy template (Fig. 4A). Therea of maximum overlap was situated in subcortical regions ofhe right hemisphere (see yellow–red coloured voxels), notablyn the right posterior insula and putamen (see Karnath et al.,004, 2005). Next, we compared lesions in patients showingore severe neglect on standard clinical tests (n = 8, see above)

elative to those with milder neglect (n = 5), using voxelwisehi-square statistical analysis in MRIcro. Neglect severity wasssessed using the same scores as in the previous section (seebove), to distinguish between two groups based on perfor-ance on neglect tests. As shown in Fig. 4B, those patientsith more severe neglect showed greater damage to the poste-

ior temporal and inferior parietal regions (orange–red colouredoxels); whereas patients with moderate neglect showed morerequent lesions in anterior frontal sites and subcortical areasblue–violet coloured voxels). These data are consistent withlassical findings of more frequent spatial neglect after damageo the temporoparietal junction (Heilman, Watson, Valenstein,

Damasio, 1983; Mort et al., 2003; Vallar & Perani, 1986;allar, 2001); and thus also indirectly supports the validity of
ur exploratory anatomical analysis.
Finally, we performed a similar analysis but now comparingatients showing the greatest facilitation by emotional facialxpression (n = 6), with those showing a smaller facilitation

N. Lucas, P. Vuilleumier / Neuropsychologia 46 (2008) 1401–1414 1409

Fig. 4. Anatomy of brain lesions in neglect patients: voxelwise reconstruction using MRIcro. (A) Areas of lesion overlap across all patients are shown on axial slicesof a normalized magnetic resonance imaging brain template. Colours code for the number of patients with damage to a given area (from 1 = violet to 13 = red). (B)Comparison of severe neglect vs. mild neglect using a voxelwise χ2 subtraction analysis: patients with severe neglect symptoms had more frequent lesions in moreposterior areas, encompassing superior temporal and inferior parietal areas (red–orange); whereas those with mild neglect symptoms had more frequent lesions infrontal lobe (blue–green). The colour bar represents χ2 values from −9 (blue) to +3 (red) for voxels involved more often in cases with severe vs. mild neglect. (C)C ion onj erease e) tof

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omparison of patients showing large vs. small benefits from emotional expressunction were associated with larger effects of emotional cues (red–orange); whmotional cues (blue). The colour bar represents chi-square values from −6 (bluacilitation.

n = 7). For this comparison, we separated patients in two groupsased on a median-split of their RT difference between theeutral (ID-only) and emotional face targets (using the meanf ID + FEAR and ID + HAP, or either emotion alone, did nothange the results). This difference provides an index reflect-ng the sensitivity to emotional facial cues during search. Asllustrated in Fig. 4C, this mapping analysis revealed more fre-uent lesions in inferior temporal and parieto-frontal cortexn patients showing strong benefits of emotional expressionsred–orange voxels); whereas patients showing less facilitationy emotional facial expression had posterior orbitofrontal areasore frequently damaged (blue–violet voxels).

. Discussion

.1. Intact pattern of cueing effects on visual search ineglect

Our study demonstrates for the first time that, despite rightemisphere damage and abnormal spatial biases in attention,isual search in neglect patients is still reliably influencedy emotional expression in faces as well as by colour cues.n this task, healthy subjects showed significant benefits byask-irrelevant, but distinctive, attributes of faces (colour and
xpression), indicating that these attributes contributed to makehe targets more salient and drew attention more efficiently toheir location. Facilitation was the strongest with colour cues,onsistent with classic “pop-out” effects normally found when
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target detection RTs during face search. Lesions in posterior temporo-parietalanterior lesions in orbitofrontal regions were associated with smaller effects of+6 (red) for voxels involved more often in cases with small vs. large emotional

he target and distracters differ along a simple visual featureTreisman & Gelade, 1980; Wolfe & Horowitz, 2004). However,earch was also reliably facilitated by the emotional expressionf target faces, consistent with previous findings in normal sub-ects showing that attention is more readily oriented to emotionalhan neutral stimuli (Eastwood et al., 2003; Fox et al., 2001;ourtois, De Pretto, Hauert, & Vuilleumier, 2006). Emotionalues speeded the detection of a target face singleton, relativeo a neutral target face to a somewhat lesser extend, as com-ared to colour cues, consistent with the fact that more subtleistinctive attributes must be processed in the case of expres-ion relative to colour cues (Duncan & Humphreys, 1989; Wolfe

Horowitz, 2004). This pattern of results in healthy subjectsccords with the view that different salient properties of visualtimuli can be used to guide the deployment of attention, and thathese do not only involve basic features coded at early stages ofisual processing but also more abstract properties, e.g. asso-iated with stimulus category and affective meaning (Mack,appas, Silverman, & Gay, 2002; Ro et al., 2001), with the for-er low-level influences being generally more efficient than the

atter high-level (Wolfe & Horowitz, 2004). Moreover, we alsoound that search for faces was generally more efficient in lefthan right space in healthy subjects, in keeping with the well-nown left visual field/right hemisphere preferences for face
rocessing in humans (Landis, Assal, & Perret, 1979; Pourtois,e Pretto et al., 2006), and further suggesting that attention wasuided by face processing mechanisms rather than just low-levelerceptual mechanisms.

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Remarkably, despite considerable slowing and contralesionalnattention, neglect patients also exhibited significant cueingenefits with both the colour and expression of faces, and theseffects were similar to those found in healthy subjects (compareigs. 2 and 3). Thus, although generally slower to find targetaces on the left than the right side, patients were faster to detectface with a different colour or a different expression, relative

o a face with similar colour and neutral expression as the dis-racters, regardless of target side. Even when taking into accounthe slowing of RTs in neglect patients, the relative magnitude ofacilitation by colour “pop-out” and by emotional expressionas comparable to that found in healthy subjects, as demon-

trated by similar RT ratios for the cued relative to the neutralonditions ([RTID-only − RTcue]/RTID-only) in both groups (seeable 3). This RT advantage was paralleled with similar effectsn accuracy rates in the patients. The fact that for both RTs andccuracy, cueing effects were symmetrical and did not inter-ct with target side, despite left neglect, strongly suggest thatoth the colour and emotional cueing mechanisms could stillffectively guide attention to distinctive targets on both sides ofpace.

The preserved facilitation by colour in this search task (simi-ar to the classic “pop-out” effect) indicates that some processingf the colour singleton was still taking place on both sidesf space in neglect patients. Several studies on visual search,sing different stimuli, have reported similar results, and sug-ested that single feature search is preserved in both visualelds in parietal patients with neglect (Arguin, Cavanagh, &oanette, 1994; Aglioti et al., 1997; Esterman et al., 2000); aesult interpreted as showing intact “parallel” processing of stim-li at early “pre-attentive” stages in the visual system. However,ther authors found significant deficits in single feature searchn neglect patients, with impaired detection of “pop-out” tar-ets (e.g. colour singleton) in contralesional space (Behrmann,bert et al., 2004; Pavlovskaya et al., 2002). Such findingsuggest instead that orienting towards these “pop-out” stimuliight recruit the same attentional mechanisms as those medi-

ting serial search for more complex (e.g. conjunction) targets,ather than proceed in “parallel” without attention across bothisual fields. In our paradigm, we did not directly compare par-llel vs. serial processes in search, but found that neglect patientsere slower to detect target faces on the left side relative to the

ight side, even when cued by a “pop-out” colour difference (seeig. 3). This agrees with some dependence on spatial attentionor orienting to and reporting these targets (Behrmann, Geng,

Shomstein, 2004; Joseph, Chun, & Nakayama, 1997), whichas protracted towards the contralesional side in the patients.ere, however, by comparing different types of cues, we show

hat a colour singleton can induce a relative facilitation that doesot entirely overcome or abolish the effect of left inattention; butnstead such facilitation can modulate search efficiency and pre-umably reflects distinct visual processes, which remain intactespite spatial attention deficits. Accordingly, some residual pro-
essing of colour might still arise in extrastriate visual areasBartels & Zeki, 2000) that are spared by brain damage in neglectatients (Driver & Vuilleumier, 2001; Vuilleumier, Valenza, &andis, 2001).
its

hologia 46 (2008) 1401–1414

A remaining question concerns the “selectivity” of these emo-ional influences on stimulus detection, that is, whether these

ay affect the detection of the emotionally laden items but notther neutral stimuli presented at nearby locations (or perhapsverlapping with them) in left space. This issue may warrantome further testing with a different paradigm than classic visualearch, as used here, and would allow to determine whether emo-ional signals influence space-based or object-based allocationf attentional resources.

.2. Additive effects of emotional cues on spatialttentional biases

The most novel and important finding of our study was theact that emotional facial expressions could also facilitate detec-ion of face targets during visual search, with similar benefitsbtained in both the contralesional and ipsilesional space. Thesendings go beyond previous results showing reduced visualxtinction for emotional stimuli in neglect patients (Vuilleumier

Schwartz, 2001b; Fox, 2002) or affective priming with extin-uished contralesional emotional faces (Williams & Mattingley,004), by demonstrating here that such emotional effects canperate in a difficult search task with a more cluttered visualcene and many competing distracters. Moreover, these cueingffects by emotional expression cannot be simply explained byystematic low-level perceptual variances, as shown by pixel-ise analyses of dissimilarity on our stimulus set (see Section 2)

hat indicated that the variance in image content due to emotionalxpression differences was negligible relative to the variance dueo identity (and/or gender) differences (see also Juth, Lundqvist,arlsson, & Ohman, 2005; or Ohman, Lundqvist, & Esteves,001).

Critically, our findings also demonstrate for the first timehat these emotional effects on attention may have the samestrength” bilaterally across visual space, despite neglect.hus, the facilitation by emotional cues did not interactith face location and was present regardless of neglect

everity. Further, the relative ratio of cueing effects (i.e.RTID-only − RTcue]/RTID-only) was strikingly comparable ineglect patents to those in healthy controls (Table 3). Thisattern of facilitation strongly suggests that the effect of emo-ional expression on visual search was essentially additive tohe pathological biases in spatial attention, with similar cue-ng influences on both the contralesional and ipsilesional targetsespite a general deficit in orienting towards the contralesionalpace. Our data therefore provide new support to the viewhat emotional influences on visual attention might have dis-inct sources, presumably related to affective processing withinimbic brain systems, rather than top-down control from atten-ional networks in fronto-parietal areas (Amaral, Bauman etl., 2003; Vuilleumier, 2005). Such emotional influences mayemain relatively intact in neglect patients, despite the largeight-hemispheric damage in the middle cerebral artery territory.

Neuroimaging findings in normal subjects typically showncreased activation of visual cortex to emotional stimuli relativeo neutral stimuli, including faces with fearful or happy expres-ion (Morris, Friston et al., 1998; Pessoa et al., 2002; Vuilleumier

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t al., 2004). It is generally thought that such increases may beriven by direct feedback from the amygdala on visual areasAmaral, Bauman et al., 2003; Vuilleumier, Armony, Driver, &olan, 2003; Vuilleumier et al., 2004). These neural circuitsere anatomically intact in our patients and might be respon-

ible for boosting visual responses to emotional faces. Suchncreases could provide a likely neural substrate for guidingttention more efficiently to the location of salient emotionaltimuli, and partly compensate for spatial biases due to pari-tal lesions. In keeping with this, previous fMRI results in aatient with right parietal damage and left visual extinction havehown that fusiform cortex may still respond to faces and facialxpressions without conscious awareness (Vuilleumier, Armonyt al., 2002). In this patient, amygdala and orbitofrontal areasere also selectively activated by fearful expressions without

wareness. Similarly, covert activation of amygdala and relatedmotional circuits may arise in patients with cortical blindnessde Gelder et al., 1999; Morris et al., 2001; Pegna et al., 2005), ornder certain conditions with masked stimuli in normal subjectsLiddell et al., 2005; Morris, Ohman, & Dolan, 1998; Whalent al., 1998; but see also Pessoa, Japee, & Ungerleider, 2005),uggesting that some emotional processing might be elicitedrior to full attention and awareness of the stimuli, and henceerve to guide attention more preferentially towards these salientvents.

Interestingly, by exploring the possible impact of differentesion sites on performance in individual patients, we found thatamage to fronto-parietal areas was associated with more severeeglect (as expected), but strikingly also with stronger benefitsf cueing by face expression. Patients who took the greatestdvantage of emotional facial cues had lesions that affectedore frequently posterior parietal, lateral prefrontal, and inferior

emporal areas. By contrast, patients who showed less facilita-ion by emotional facial expression had lesions more frequentlyxtending into orbitofrontal cortex (OFC). This finding mightndicate that limbic prefrontal cortex is critically implicated in

ediating the facilitatory effect of emotional cues on atten-ion as observed here. OFC is anatomically closely related,nd functionally strongly connected, to the amygdala (Cavada,ompany, Tejedor, Cruz-Rizzolo, & Reinoso-Suarez, 2000).lthough our anatomical analysis must be regarded as prelim-

nary due to the small sample of patients, a similar correlationest between lesions and neglect signs in our patients showed areater involvement of inferior parietal and posterior temporalegions in those with more severe neglect, as predicted by pre-ious neuroanatomical studies (Karnath et al., 2004; Mort et al.,003; Vallar, 2001). OFC is known to play a critical role in emo-ional processes, not only receiving direct inputs from amygdala,ut also projecting to several cortical regions in frontal, pari-tal, and extrastriate visual areas (Cavada et al., 2000). Damageo OFC, or to the connections between limbic areas and otherrain regions, might possibly disrupt the modulatory effects ofmotion on visual perception and spatial attention. By contrast,
esions in parietal and lateral prefrontal areas, more directlymplicated in classic spatial attention processes, might not onlyeave emotional influences relatively intact, but perhaps makehem become even more apparent due to the reduced control by
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hologia 46 (2008) 1401–1414 1411

op-down attentional processes (Yamasaki, LaBar, & McCarthy,002).

Notably, in another recent study in a different samplef neglect patients (Grandjean, Sander, Lucas, Scherer, &uilleumier, 2008), we found that emotional cues in voices

prosody) can also reduce contralesional auditory extinction, buthese emotional effects were again stronger when posterior OFCas intact, just as we found here. Further studies should inves-

igate more precisely the role of OFC in attentional guidance.n any case, our preliminary anatomical findings provide someonvergent evidence for the view that enhanced orienting tomotionally salient stimuli may be driven by distinct processes,ndependent from (and additive to) the control implemented byttentional systems in parieto-frontal areas.

Finally, our results indicate that emotional influences onearch may not only arise for fearful faces, but also for happyaces, suggesting that facilitatory effects are not restricted toegative or threat-related stimuli (Juth et al., 2005; Ohman &oares, 1998). Previous research on behavioural (Fox, 2002;undqvist & Ohman, 2005; Mogg & Bradley, 1999; Ohman,lykt et al., 2001) and neural (Vuilleumier et al., 2004; Pourtois,chwartz, Seghier, Lazeyras, & Vuilleumier, 2006) effects ofmotion on attention has often focussed on negative cues, dueo the strong involvement of amygdala circuits in fear-relatedrocesses. However, positive or reward-related cues have alsoeen reported to influence visual attention (Fenske & Eastwood,003; Williams, Morris, McGlone, Abbott, & Mattingley, 2004;illiams et al., 2005), and can also increase activation in both

mygdala and visual cortical regions (Pessoa, Japee, Sturman, &ngerleider, 2006; Sabatinelli, Bradley, Fitzsimmons, & Lang,005; Winston, O’Doherty, & Dolan, 2003). Attentional biasesave also been found to be elicited by baby faces that representighly arousing and biologically relevant, but not threateningtimuli (Brosch, Sander, Pourtois, & Scherer, in press; Brosch,ander, & Scherer, 2007). This pattern is therefore consistentith theoretical proposals that the appraisal of both negative

nd positive events should act on attentional processes to con-rol awareness and ongoing behaviour (Scherer, 2001; Sander,rafman, & Zalla, 2003).

. Conclusion

The present study has extended previous findings about resid-al processing of salient visual cues during visual search ineglect patients, and demonstrated that visual search can beodulated by emotional biases, over and above spatial biases

n attention caused by right hemisphere damage. Our data pro-ide new answers to current questions concerning interactionsetween attention and emotion (Phelps, Ling, & Carrasco, 2006;essoa et al., 2002; Vuilleumier, 2005). We show that emotional

nfluences on search may exert purely additive facilitation of tar-et face detection on both sides of space, and that these effectsissociate from attentional biases due to parieto-frontal damage
nd do not interact with neglect severity. In the future, fruitfulpplications might exploit such residual processing in emotionalnd motivational systems to develop new therapeutic programsor patients suffering from spatial neglect.

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cknowledgment

The authors thank Dr. K. N’Diaye for help on low-level stim-lus analysis.

This work was supported by a grant from the Swiss Nationalcience Foundation to Prof. Patrik Vuilleumier (632.065935).

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