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nilateral damage to the right cerebral hemisphere disrupts thepprehension of whole faces and their component parts
avid Wilkinsona,b,c,∗, Philip Koa,b, Antonius Wiriadjajaa,b, Patrick Kilduff a,b,egina McGlincheya,b, William Milberga,b
Geriatric Neuropsychology Laboratory, New England Geriatric, Research, Education & Clinical Center, Veterans Affairs Boston Healthcare System, USADepartment of Psychiatry, Harvard Medical School, USADepartment of Psychology, University of Kent, UK
r t i c l e i n f o
rticle history:eceived 14 February 2008eceived in revised form 13 January 2009ccepted 4 February 2009
a b s t r a c t
Although most cases of acquired prosopagnosia are accompanied by bilateral brain lesions, a number alsoarise following right unilateral lesions. The prevailing consensus is that right hemisphere damage disruptsthe configural apprehension of faces, which in turn forces a reliance on part-based processing. Here we
vailable online 11 February 2009
eywords:rosopagnosiaonfiguraleatural
describe a patient who following right hemisphere damage is not only unable to apprehend the configuralaspects of faces, but is also unable to apprehend their component parts when these are presented withina whole, upright face. Intriguingly, the patient is able to apprehend face parts when these are presentedin isolation, within inverted faces, or in unfamiliar, scrambled arrangements. Furthermore, the patientcan make use of configural information to detect local changes in non-face stimuli. The findings uncovera hitherto unreported form of impairment following right unilateral damage, and raise questions about
here
nversion superiority the role of the left hemisp
. Introduction
Patients with prosopagnosia are able to classify a face as a ‘face’,ut are unable to recognize it as familiar (Bodamer, 1947). The dis-rder may arise through a failure to either construct an adequateerceptual representation of the face (apperceptive prosopagnosia)e.g. Boutson & Humphreys, 2002), or access higher-level seman-ic information (associative prosopagnosia) (e.g. De Renzi, Faglioni,rossi, & Nichelli, 1991). In most cases of acquired prosopagnosia
hat have been reported, a lesion is sustained to bilateral ven-ral occipito-temporal cortex (Damasio, Damasio, & van Hoessen,982; Meadows, 1974). This region incorporates dense networksf face responsive neurons, many of which are contained withinhe middle fusiform gyrus (Sorger, Goebel, Schiltz, & Rossion,007). However, a small number of neuropsychological studiesuggest that a right hemisphere lesion is in fact sufficient forrosopagnosia (Barton, 2008; De Renzi, 1986). In these less com-
on cases, the precise nature of face processing impairment is
nclear.The idea that prosopagnosia can result from a right cerebral
esion was first proposed from post-mortem studies (Assal, 1969;
∗ Corresponding author at: Department of Psychology, University of Kent, Can-erbury, Kent CT2 7NP, UK. Tel.: +44 1227 824772; fax: +44 1227 827030.
De Renzi, 1986; Hécaen, de Ajuriaguerra, Magis, & Angelergues,1952; Lhermitte & Pillion, 1975; Meadows, 1974; Michel, Perenin,& Sierhoff, 1986; Torii & Tamai, 1985; Whiteley & Warrington,1977). However, given the typically long interval between symptomonset and death, it proved difficult to establish a causal associationbetween lesion and clinical presentation. Stronger precedent wasset by Landis, Regard, Bliestle, & Kleihues (1988) who autopsied anindividual who had acquired prosopagnosia only ten days beforedeath. In line with previous studies, the patient bore a unilaterallesion confined to the lower, posterior part of the right hemisphere.The advent of magnetic resonance imaging has since corroboratedthis finding (Barton, Press, Keenan, & O’Connor, 2002; Joubert et al.,2003; Takahashi, Kawamura, Hirayama, Shiota, & Isono, 1995; Wada& Yamamoto, 2001), and also allowed for a more precise delineationof the brain regions that are critical for face recognition (see Uttner,Bleim, & Danek, 2002; Wada & Yamamoto, 2001).
From a cognitive perspective, the question arises as to why theright hemisphere is so critical for face recognition. Clues arise froma wide variety of both normative and neuropsychological studieswhich indicate that the individuation of a face strongly relies onconfigural, as opposed to part-based, styles of information process-
ing. By the term ‘configural’, we refer either to the second-orderrelations that describe the way in which face parts are arranged(Murray, Yong, & Rhodes, 2000) or to the holistic idea that individ-ual parts are not explicitly represented and instead coded only tothe extent that they contribute to the overall identity of the face
R.C showed neglect in two SCAN sub-tests: in the bisection task he produceda mean left-sided deviation of 1.6 cm (8%), and in the extinction task he missed agreater number of right-sided targets (37%) compared to left-sided targets (16%)under double-simultaneous (i.e. bilateral) presentation. An additional test alsorevealed the presence of a lateralized visual search deficit. When searching for an
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Farah, Wilson, Drain, & Tanaka, 1998), Either way, the pattern oferformance seen in patients with right-sided lesions suggests thathe right hemisphere is specialized for configural styles of process-ng. For example, Landis et al. (1988) reported a patient who wasble to name individual face parts when these were presented oneparate pieces of card, but was unable to assemble them into aoherent whole. Along similar lines, Barton (2008) reported a groupf right unilateral patients whose face matching ability was muchetter when instructed to focus on a specific part of the face ratherhan on its entirety. Joubert et al. (2003) showed a similar cuingffect in a patient suffering from right anterior temporal lobe atro-hy. One conclusion that has been drawn from these studies is thathe right hemisphere induces prosopagnosia by eliminating con-gural processing, which in turn forces a reliance on less efficientart-based procedures that presumably reside in the undamaged
eft hemisphere (see de Gelder & Rouw, 2001; Rossion et al., 2000).The idea that both hemispheres contribute, albeit unequally, to
ace perception finds support outside the clinical setting. Functionalrain imaging studies show that face judgments relying on whole-ased matching preferentially activate right hemisphere, while
udgments relying on part-based matching preferentially activateeft hemisphere (de Gelder & Rouw, 2001; Rossion et al., 2000).isual half-field studies show a general left visual field-right hemi-phere superiority for configurally matching upright faces that isliminated by inversion, and a right visual field-left hemisphereuperiority for matching faces that differ by only a single featureHillger & Koenig, 1991). Intracranial ERP recording shows thathile regions of the right hemisphere respond faster to upright
aces, regions of the left respond faster to inverted faces (McCarthy,uce, Belger, & Allison, 1999). These findings mirror the cerebralsymmetries that have been found during Navon letter tasks (Delis,obertson, & Efron, 1986) and fit with the broader notion that theerebral hemispheres differ in their sensitivity to the global andocal spatial scale of many kinds of stimuli (Hellige, 1986).
In the present study, we sought to further examine the roles ofhe right and left cerebral hemispheres in processing the configuralnd featural aspects of faces. While all previous cases of right hemi-phere prosopagnosia have been explained by a loss of configuralrocessing and subsequent reliance on part-based processing, theatterns of impairment observed in several bilateral patients sug-est that right hemisphere damage could, in theory, compromiseonfigural processing in another way. Intriguingly, several bilateralatients suffer from a configural impairment that not only affectsheir comprehension of faces wholes, but also their comprehensionf face parts when these are arranged in a familiar configuration (deelder & Rouw, 2000a, 2000b; de Gelder, Bachoud-Lévi, & Degos998; Farah, Wilson, Drain, & Tanaka, 1995; Rouw & de Gelder,002). The basis to this claim comes from the paradoxical inver-ion effect which is characterized by a greater ability to identifyocal changes to faces when familiar configural cues are minimizedia inversion. This paradoxical effect not only shows that configuralrocessing is abnormal, but also demonstrates that configural pro-essing has not been eliminated because if this were so then therehould be no inversion effect at all. Instead, configural processingtill operates but in a way that interferes with the recovery of facearts. In line with this idea, individuals who show a paradoxical
nversion effect are also better at judging face parts in other taskshen these are presented in isolation or in a scrambled, unfamiliar
ormat (de Gelder & Rouw, 2000a).Given the relative scarcity of individuals who present with
rosopagnosia after unilateral right hemisphere damage, it is not
asy to establish whether the configural–featural interference seenn bilateral patients could in fact be the result of right-sided dam-ge. The issue is however important if it is to be established whetheright hemisphere damage simply impairs configural processing andorces a greater reliance on less efficient part-based routines, or
logia 47 (2009) 1701–1711
whether in fact it can disrupt both configural and featural process-ing.
In the following sections we describe four experiments that wereconducted on a prosopagnosic whose lesion is confined to the rightside of his brain. In Experiments 1 and 2 we used the face inversionparadigm to show that he is unable to utilize the familiar con-figural cues afforded by faces. More important, we show that thepresence of these cues severely degrades his apprehension of indi-vidual face parts. In Experiment 3, we administered a whole–partmatching paradigm to provide further evidence that he is unableto discriminate face parts when these are presented in a canonicalarrangement. In Experiment 4, we provide preliminary evidencethat this deficit does not extend to non-face stimuli.
2. General method
2.1. Case presentation
The patient, R.C., is a 65-year-old right-handed male who suffered a right cerebralvascular accident (CVA) in 1983 while lifting a heavy object. Prior to the stroke hewas healthy although his family history was positive for CVA in his mother andmaternal grandmother. He initially presented with a dense left hemiplegia, speechdysarthria, left hemianopia with central sparing,1 marked left-sided neglect andcould not follow sequential commands.
Initial CT revealed an embolic infarct with large vessel occlusion of the right mid-dle cerebral artery (MCA) (for other cases of prosopagnosia following right MCA seeRössler, Lanquillon, Dippel, & Braune, 1997). A carotid angiogram also revealed a rightcarotid arterial thrombosis which was either secondary to that seen in the middlecerebral artery or the result of a carotid dissection. A recent MRI scan revealed a largeright hemisphere lesion involving nearly all of the temporal lobe (see Fig. 1). Basedon Duvernoy (1999), the three, core, structural elements of the human face percep-tion system (see Haxby, Hoffman, & Gobbini, 2000) were differentially affected; (i)the inferior occipital gyrus, which contains the lateral occipital face area, appearedintact (see Fig. 1a), (ii) the fusiform gyrus also appeared intact, though all underlyingwhite matter had been destroyed leaving it both de-afferented and de-efferentedfrom other areas (see Fig. 1b), and (iii) the superior temporal sulcus was severelyimpacted (see Fig. 1a and b). The lesion continued superiorly into the lower two-thirds of the pre-motor, motor and sensory cortices, all of the supramarginal andangular gyri, and all of the white and peri-ventricular white matter beneath. Por-tions of the centrum semiovale and superior parietal lobe were also compromised.Anteriorly, the infarct included all of the inferior frontal gyrus, and extended to theunderlying white matter across to the frontal horn, interrupting fibres of the medialsubcallosal fasciculus. The anterior and posterior limbs of the internal capsule, thehead of the caudate and most of the thalamus were also lesioned. There was no signof any left hemisphere damage.2
R.C. has recovered from most of his initial symptoms, and lives by himself withthe assistance of a part-time maid. He spends much of his time reading and typingjournalistic articles though this is hampered by a persistent hemiparesis and mildleft-sided inattention (see Wilkinson, Ko, Milberg, & McGlinchey, 2008). AlthoughR.C. reports being able to categorise faces according to gender and age, he continuesto report severe difficulty in identifying the faces of even his most familiar relatives(see also Wilkinson, Ko, Kilduff, McGlinchey, & Milberg, 2005). Curiously, he appearsuntroubled by perceptual and recognition tasks that do not involve faces. Thesebehaviours were reflected in his performance on a range of standardized objectand face tests that were conducted during initial screening (see Table 1), and pointtowards an apperceptive deficit.
Given reports that R.C. suffers from left-sided inattention, it was important toestablish the extent of this impairment so that our experiments could be designedin way that minimized any impact on matching performance. A formal assessmentwas therefore carried out using the Standard Comprehensive Assessment of Neglect(SCAN) (McGlinchey-Berroth et al., 1996). The battery includes manual line bisection,letter and symbol cancellation, line crossing, complex figure and scene copy and acomputerized ‘extinction’ task. In the extinction task, one or two asterisks appearsimultaneously for 150 ms either in one or both corners of one side of the screen(unilateral trials), or on both sides of the screen either both at the top or bottom, ordiagonally opposite (bilateral trials). The patient is required to verbally indicate thelocation of dots. Neglect is inferred if evident on at least two of the subtests.
1 Further perimetry has not since been performed.2 We thank Prof. Michael Alexander and Dr. Carole Palumbo for reading the CT
and MRI films.
D. Wilkinson et al. / Neuropsychologia 47 (2009) 1701–1711 1703
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Fig. 1. MRI coronal images of R.C.’s brain with arrows showing int
pright T set amongst heterogeneously oriented distracter Ts, R.C. missed 24% ofeft-sided targets compared to 12% right-sided targets. These rates were much higherhan those observed in a group of age-matched controls who missed just 7% of tar-ets in either visual field. R.C.’s visual field asymmetry was also evident in the RTata; search was performed at a rate of 266 ms per item in left visual field comparedo 115 ms per item in the right visual field. By contrast, the age-matched controlsenerated search slopes of 135 and 97 ms per item in left and right visual fieldsespectively (for further details see Wilkinson et al., 2008).
.2. Procedures
Stimulus presentation was controlled via PsychLab (Gum, 2003) on a Macin-osh G4 laptop computer. Each experiment was preceded by a brief practice sessiononsisting of 10–20 trials. In all experiments, trials began with a 500 ms central fix-tion cross, followed by a 500 ms interval and then the experimental stimuli whichppeared on a light, grey background in the middle of the screen. The inter-trial inter-al was always 2000 ms. All experiments involved a 2AFC button-press response
ith each response type occurring randomly but the same number of times. Par-
icipants were instructed to respond as accurately and quickly as possible. In ordero minimise the effects of R.C.’s neglect and suspected hemianopia, the mapping ofach response type to each of the two response buttons was counterbalanced acrosslocks, and the two response buttons were always vertically aligned. In Experimentsand 2, the target appeared to the left and right of the screen with equal probabil-
ht inferior occipital gyrus (a), and intact right fusiform gyrus (b).
ity while in Experiments 3 and 4 all stimuli appeared centrally. At the start of eachblock, the participant was reminded of his difficulty in perceiving left-sided stimuliand urged to inspect both left and right sides of each stimulus before responding.To further lessen the effects of any lateralised impairment, the centre of the com-puter screen and two response buttons were spatially aligned with the patient’smid-sagittal plane.
The controls were right handed and had normal or corrected-to-normal vision,with no history of neurological or psychiatric illness. Different control participantswere recruited for each experiment, and were closely matched to the patient’s age atthe time of testing (65) and education (17 years): Experiment 1 = 11 controls, meanage 61, 16 years of education; Experiment 3 = 10 controls, mean age 62, 16 years ofeducation; Experiment 4 = 11 controls, mean age 61, 16 years of education.
All experiments were approved by the Boston VA Medical Centre IRB and wereperformed in accordance with the ethical standards laid down in the 1964 Dec-laration of Helsinki. All participants gave their written informed consent prior tostudy.
3. Experiment 1
In the first experiment we sought to confirm that R.C.’sprosopagnosia is linked to a deficit in configural encoding. By ‘con-figural’ we refer to either the second-order spatial relations that tie
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Table 1R.C.’s response accuracy on standard tests of recognition and matching.
FacesBenton Facial Recognition Test 15%Wechsler Memory Scale Immediate Test for Faces 48%
Famous facesFrom last 20 years 15%From last 20 to 40 years 15%
Non-facesBoston Naming Test 93%a
Birmingham Object Recognition Test (Riddoch & Humphreys, 1993)Perceptual matching
Length 87%a
Size 90%a
Orientation 80%a
Position of gap 93%a
Access to structural descriptionsForeshortened feature match 92%a
Minimal feature match 88%a
Access to stored knowledge
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Object decision—easy 88%a
Object decision—hard 72%a
a Accuracy within 2 standard deviations of the control mean.
he individual parts of an object together (Murray, Yong, & Rhodes,000), or to the idea that individual parts are not explicitly repre-ented and instead coded only to the extent that they contributeo the overall identity of the face (Farah et al., 1998). In either case,hese more global attributes are thought to more clearly individuateaces than their component parts.
A simultaneous matching task was administered in which theatient and a healthy control group reported which of two hori-ontally aligned faces matched a sample face positioned directlybove. On each trial, faces were either all upright or all upsideown and the arrangement of the eyes, nose and mouth wasither normal or scrambled into an unfamiliar configuration. Thesetimulus manipulations gave rise to four experimental conditions:1) normal feature arrangement, upright orientation, (2) normaleature arrangement, inverted orientation (3) scrambled featurerrangement, upright orientation, (4) scrambled feature arrange-ent, inverted orientation. On any given trial, one of the probes
xactly matched the sample face. The other face differed only inhe orientation of the eyes and mouth. These local changes cre-te the so-called ‘Thatcher illusion’ (Thompson, 1980) in which theace appears grotesque when upright but quite usual when turnedpside down (see Fig. 2a).
Three particular aspects of the task allowed us to assess thentegrity of R.C.’s face processing. First, if R.C. is able to apprehendace parts when these appear in their usual canonical arrangementhen he should be able to detect changes in whole, upright thatcher-zed faces, since faces mainly differed in the orientation of the eyesnd mouth relative to other parts, as opposed to the identity of thendividual parts themselves (see Boutson & Humphreys, 2002). Sec-nd, if R.C. has intact configural processing then his apprehensionf face parts should be facilitated when these appear in a familiarpright format, relative to when they appear upside down (Rhodes,rake, & Atkinson, 1993; Yin, 1969). Third, he should be worse atatching faces that are scrambled compared to normally config-
red because, as with inversion, familiar configural cues are noonger available to assist in the apprehension of face parts.
.1. Method
10 digitized grey-scale images of male faces were taken from theace database provided by the Max-Planck Institute for Biologicalybernetics, Tuebingen, Germany. In the normally arranged con-
logia 47 (2009) 1701–1711
dition, a variant of each stimulus was produced by inverting themouth and eyes. To produce stimuli in the scrambled condition, thefirst-order relations between the eyes, mouth and nose were alteredin each of the 10 faces. The nose and mouth could appear eitherabove or below their original positions, which in some instances ledto the nose appearing below the mouth. Each eye was moved to anew position in the face with the constraint that it always remainedon its original side. Local image incongruities that resulted frommoving the parts around were removed by using the blurring toolin the graphics software used to manipulate the images. As in thenormally arranged condition, a variant of each scrambled face wasproduced by inverting the mouth and eyes.
Each trial consisted of 3 faces with the sample appearing abovetwo laterally aligned images of its duplicate and a thatcherisedcounterpart. The lateral position of the target was counterbalancedacross trials. All 3 faces appeared upright for half the total num-ber of trials and upside down for the remainder. Participants weretold to choose which of the bottom two faces, ‘left’ or ‘right’ exactlymatched the top, sample face. Pictures appeared for 3500 ms afterwhich there was a blank screen lasting until a response was made.On any given trial, the faces could be arranged in either a normalor scrambled configuration and were upright or inverted. Each nor-mally arranged face served twice as the sample image in the uprightand inverted conditions, generating a total of 80 trials.
3.2. Results
The patient’s and controls’ error scores were analyzed inseparate 2 (Feature Arrangement: normal vs. scrambled) × 2 (Ori-entation: upright vs. inverted) repeated measures ANOVAs. Toprovide a measure that was free of response bias, d′ scores were alsocalculated and used to generate 95% prediction intervals from thecontrol group data. As in all experiments reported, post hoc compar-isons were conducted using either planned or corrected pair-wisecomparisons, and all reported effects are Greenhouse-Geisser cor-rected. There were too few correct trials (<10 data-points) in thepatient’s upright condition to conduct a meaningful RT analysis.Accordingly, the control RT data are not shown.
3.2.1. ControlsErrors: The main effects of Orientation (F(1,10) = 11.6, p < 0.05)
and Feature Arrangement reached significance (F(1,10) = 34.6,p < 0.05). Upright faces were judged more accurately than invertedfaces, and normally arranged faces were judged more accuratelythan scrambled faces. The interaction term was not significant(F < 3.1).
3.2.2. PatientThe main effect of Orientation (F(1,19) = 15.6, p < 0.05), and
the interaction between Orientation and Feature Arrangement(F(1,19) = 12.7, p < 0.05), both reached significance (see Fig. 2b).Paired t-tests (˛ = 0.01) showed that upright intact faces wereharder to judge than the three other stimulus types, and alsorevealed a significant advantage for judging normally arrangedinverted faces over scrambled upright faces. The difference betweennormally arranged, inverted faces and scrambled, inverted facesapproached significance (p = 0.07). There was no effect of inversionacross the two scrambled conditions.
3.3. Signal sensitivity d′
The patterns of error shown by the patient and controls werereflected in their corresponding d′ scores which are summarised inTable 2.
As a further means of establishing the unusualness of R.C.’sinversion superiority effect, we calculated an inversion index
D. Wilkinson et al. / Neuropsychologia 47 (2009) 1701–1711 1705
Fig. 2. Example probe faces presented in Experiment 1. On any given trial, participants had to decide which of two probe faces matched a sample face presented directlyabove. One of the probe faces was exactly the same as the probe (see ‘same’ faces in figure) while the other had been thatcherised (see ‘different’ faces in figure) (a). Associatedmean %error with standard deviation bars (b).
Table 2Patient and control group d′ scores, showing 95% prediction intervals for the control data.
a Scores that fall inside the lower limit of the control prediction intervals.
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706 D. Wilkinson et al. / Neurop
(upright − inverted)/(upright + inverted)] from his upright andnverted d′ scores and then looked to see if this fell inside the 95%rediction interval of the control group’s inversion index. R.C.’s
ndex for normally arranged faces (−2.1) fell outside the normalange (upper 1.0, lower −0.02), while his inversion index for scram-led faces (−0.3) fell inside it (upper 1.7, lower −0.7).
.4. Discussion
The key finding is that, unlike the healthy controls, R.C. failed tohow an advantage for normally arranged, upright faces. In fact, hehowed a paradoxical inversion effect whereby his matching of nor-ally arranged faces was actually better when these were inverted
han upright. Compellingly, the prediction intervals indicate thatis performance in the inverted condition was indistinguishable
rom that of the controls. This suggests that R.C. has not lost thebility to encode individual face parts because if this were so thenis performance would remain at chance regardless of orientation.
t also suggests that he has not lost the ability to process configu-al relations because if this were so then he would show no effectf inversion. Rather, it suggests that his configural processing isamaged but continues to operate in a way that interferes with theecovery of part-based information.
Inversion superiority has been reported in three bilateralatients (de Gelder et al., 1998; de Gelder & Rouw, 2000b; Farah etl., 1995), but this is the first unilateral case of which we know. Inine with these previous cases, the effect was apparent in R.C.’s accu-acy data and elevated performance well above chance. However,he conditions previously needed to bring about inversion supe-iority relied on several, procedural adjustments; computerizedorms of presentation and button press responses did not produceonsistent data while printed matter and vocal responses did,ither a delayed match-to-sample procedure and/or presentationf the probe stimuli in 3/4 plane (as opposed to frontal plane) wereequired, and different stimulus exposure durations were neededor the patient and controls. These previous studies also omittedetween-group statistical analyses making it difficult to know ifatients’ matching performance was ever normal. At this stage it isnclear whether we chose procedures that just happened to be veryensitive to R.C.’s inversion effect, or whether there is somethingbout his impairment that made it especially easy to find.
In line with his paradoxical inversion effect, R.C.’s matchingerformance also improved when familiar configural cues wereeduced via scrambling. Given that familiar configural cues wereost reduced in the inverted, scrambled condition, one might have
xpected performance in this condition to have been the most accu-ate of all; that is, even more accurate than in the normally arranged,nverted condition in which configural cues were only reduced via aingle manipulation. One possible reason why this was not the cases that the lateral asymmetry of scrambled faces exacerbated R.C.’seglect of left-sided parts (see Driver, Baylis, & Rafal, 1992). Coupledith the novel appearance of the stimuli, this may have elicited annusual matching strategy that was less efficient that that for nor-ally arranged (e.g. left-right symmetrical), inverted faces. What-
ver the actual reason, the important point is that R.C. was muchetter at matching faces when they were scrambled than upright
ntact. We also point out that previous demonstrations of the para-oxical inversion effect have not incorporated a scrambled manipu-
ation, so it remains unclear whether R.C.’s responses to the scram-led stimuli were that exceptional compared to other patients.
. Experiment 2
The paradoxical inversion effect shown by R.C. suggests thatis perception of face parts is at chance accuracy when these are
Fig. 3. Example faces presented in Experiment 2 (a), and associated mean %errorand mean correct RTs with standard deviation bars (b).
presented as part of a normally arranged, upright face, but rel-atively accurate when freed from either of these constraints. Iftrue, then his matching of upright faces should again move beyondchance when stimuli depict only the critical features (eyes andmouth) as opposed to the entire face. We tested this hypothesis inExperiment 2.
4.1. Method
A new set of faces were drawn from the face database providedby the Max-Planck Institute for Biological Cybernetics, Tuebingen,Germany, and all detail removed apart from the eyes and mouth (seeFig. 3a). All other aspects of the study were identical to Experiment1, with the exception that the scrambled condition was excludedsince there was no longer any need to control for ‘face context’.
4.2. Results
R.C. produced 20% incorrect responses for upright faces(d′ = 1.1) and 15% incorrect responses for inverted faces (d′ = 1.4)(see Fig. 3b). One-sample t-tests showed that both conditions
showed that the difference between the upright and invertedconditions was not significant, t(19) = 1.9, p > 0.05. Finally,a paired t-test of his mean correct RTs (upright = 4025 ms,inverted = 4227 ms) also failed to show a significant difference,t(15) = 0.7, p > 0.05).
D. Wilkinson et al. / Neuropsychologia 47 (2009) 1701–1711 1707
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.3. Discussion
As in Experiment 1, R.C. was able to perform part-basedatching at an above chance-level (20% errors) when normal
ace context was removed. This finding confirms that he can, inrinciple, make good use of feature-based information to per-eptually match faces but that configural information somehowmpairs this process. Given that we did not run a control group,t cannot be established whether an error rate of 20% is abnor-
ally high. But regardless of whether his part-based matching isntirely intact, the data show that his deficit is clearly exagger-ted when face parts are presented within their familiar configuralrrangement.
. Experiment 3
The aim of Experiment 3 was to seek evidence from a dif-erent paradigm for the idea that R.C.’s part-based matching isisturbed by familiar spatial cues. We therefore administered a
ciated mean %error and mean correct RTs with standard deviation bars (b).
complete versus part probe face matching paradigm which inuntrained, healthy observers typically reveals a configural supe-riority effect (Donnelly & Davidoff, 1999; Tanaka & Farah, 1993).Specifically, changes in the identity of face parts are more easilydetected when presented within a whole face probe than a partprobe.
The experiment involved brief stimulus presentations of a sam-ple face and then, after a brief delay, either another face (completeprobe) or a face part (eyes, nose or mouth) (part probe). On eachtrial, participants decided if the probe contained either the same-or different-sized part(s) to the sample (see Fig. 4a). If a com-plete probe advantage occurs then one might argue that the effectis merely ‘contextual’ in nature (see Gauthier & Tarr, 2002). Thatis, regardless of spatial arrangement, simply presenting a face
part amongst other parts leads to better recognition than whenpresented in isolation. To address this, we included a separate con-trol condition in which the complete probe was altered so theindividual parts appeared in a scrambled as opposed to familiarformat.
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.1. Method
Six sample faces were constructed, each with six complete probeounterparts that varied by the size (small, medium, large) of oneeature (eyes, nose, mouth) and six part probe counterparts inhich the altered feature was presented singularly (see Fig. 4a). Onifferent trials, there was an equal likelihood that the eyes, nose orouth had changed in size. Scrambled versions of each target and
omplete probe were generated by arranging their internal featuresnto unfamiliar configurations, as in Experiment 1.
Sample faces appeared for 6000 ms, followed by a 2000 ms inter-al, and then the probe, which remained on-screen until a responseas made. The patient pressed ‘same’ if the probe contained iden-
ical part(s) to the sample or ‘different’ if one of the features hadhanged. Each trial type appeared 36 times producing a total of 216rials. The scrambled and normal conditions were run in separatelocks, the order of which was counterbalanced.
.2. Results
The Error and RT scores for patient and controls were ana-yzed in separate one-way 3 (Probe: complete vs. scrambled vs.art) repeated measures ANOVAs. Significant effects were furtherxamined using paired t-tests with an adjusted alpha of 0.01. Asn Experiment 1, 95% prediction intervals were constructed fromhe controls’ d′ scores to directly compare aspects of the patient’sesponses to those of the controls.
.2.1. ControlsErrors: The main effect of Probe was significant (F(2,18) = 7.6,
< 0.05), such that responses to complete probes generated fewerrrors than those to either part or scrambled probes.
RT: Responses to scrambled faces were longer than to eitheromplete or part probes (F(2,18) = 54.5, p < 0.05).
.2.2. PatientErrors: The main effect of Probe was significant (F(2,70) = 5.2,
< 0.05); by stark contrast to controls, part probes generated fewerrrors than complete or scrambled probes (see Fig. 4b).
RT: The effect of probe failed to reach significance (F < 1.0).
.2.3. Signal sensitivityThe d′ scores shown in Table 2 illustrate that the controls were
oth highly and differentially sensitive to the information con-ained within the various probes. By contrast, R.C. was not especiallyensitive to this information, although his part probe performanceid just fall inside the lower limit of the relevant 95% prediction
ell outside the normal range, we generated a whole–part index(whole − part)/(whole + part)] and then compared this to the cor-esponding 95% prediction interval derived from the controls. Asxpected, R.C.’s whole–part index (−0.4) fell outside the normalange (upper limit 0.5, lower limit −0.2).
.3. Discussion
In line with Experiments 1 and 2, the failure to show a normalomplete probe advantage (CPA) points towards a visual deficit thatisrupts the coding of face parts when these are presented withinnormal face context.
Given the nature of the task, we were unsurprised that theatient performed relatively poorly in all three probe conditions.ecall that each trial began with an upright, normally configuredample face, after which one of the three probe types appeared.iven R.C.’s configural deficit, it would have been difficult to extract
logia 47 (2009) 1701–1711
useful information from the sample for subsequent matching. Thatsaid, R.C. did show an advantage for judging part probes over bothscrambled and complete probes. One reason may lie in the factthat both the complete and scrambled probes depicted whole faceswhereas the part probe depicted only a small section of face. It ispossible that the limited amount of information in the part probeallowed R.C. to more easily focus attention on the relevant facial fea-ture. In line with this explanation, other prosopagnosics becomebetter at matching face parts when pre-cued to only those fea-tures that are relevant, an effect attributed to top-down attentionalfacilitation (Barton et al., 2002; Joubert et al., 2003).
6. Experiment 4
The aim of Experiment 4 was to make an initial assessment ofwhether R.C.’s configural deficit extended to non-face objects. Wetherefore tested whether his absence of a complete probe advan-tage (CPA) for faces extended to houses. As pointed out by others,face and houses share certain visual characteristics; they both havea canonical orientation, and have discernable parts that tend tobe arranged in a particular way. Most important, Donnelly andDavidoff (1999) showed that the CPA normally shown for facesextends to house stimuli. This was taken to suggest that config-ural processes influence part-based processing in a similar way forboth kinds of stimuli.
We therefore replaced the face stimuli with non-face stimuliand re-ran the CPA experiment. If the detrimental effect of config-ural information on part-based matching reflects a more generalprocessing deficit then a CPA for houses should likewise be absent.Alternatively, if the configural deficit does not generalize to otherkinds of hierarchical stimuli then a CPA for houses should be found.
6.1. Method
Six sample houses were constructed, each with six completeprobe counterparts that varied by the size (small, medium, large)of one feature (door, windows, chimney) and six part probe coun-terparts in which the altered feature was presented singularly. Inthe scrambled condition, the individual features were re-arrangedinto unfamiliar configurations (see Fig. 5a). As before, sample stim-uli appeared for 6000 ms, followed by a 2000 ms interval, and thenthe probe, which remained on-screen until response.
6.2. Results
The Error and RT scores were analyzed in one-way 3 (Probe:complete vs. scrambled vs. part) repeated measures ANOVA. Signif-icant effects were teased apart using paired t-tests with an adjustedalpha of 0.01.
6.2.1. ControlsErrors: The main effect of probe reached significance
(F(2,20) = 10.1, p < 0.05). Paired t-tests showed that responsesto complete probes generated fewer errors than scrambled probes.However, the difference between complete and part probes wasonly significant at an alpha of 0.05 (p = 0.039). Given the strongprecedent for this effect to be significant (Donnelly & Davidoff,1999), we nevertheless felt that it would be overly conservative toclass it as non-significant.
RT: The main effect of probe reached significance (F(2,20) = 42.3,p < 0.05); part probes were responded to the fastest, followed bywhole and then scrambled probes.
6.2.2. PatientError: The main effect of probe reached significance (F(2,70) = 7.1,
p < 0.05); complete probes generated less errors than either part orscrambled probes (see Fig. 5b).
D. Wilkinson et al. / Neuropsychologia 47 (2009) 1701–1711 1709
and as
6
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w[cRu
6
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Fig. 5. Example sample and probe stimuli presented in Experiment 4 (a),
RT: The main effect of probe failed to reach significance (F < 2.5).
.2.3. Signal sensitivityThe patterns of error shown by the patient and controls were
eflected in their corresponding d′ scores depicted in Table 2. Unliken Experiment 3, 95% prediction intervals based around the controlata showed that the patient performed within the normal rangecross all three experimental conditions.
To establish whether R.C.’s whole–part advantage fellithin the normal range, we generated a whole–part index
(whole − part)/(whole + part)] and then compared this to theorresponding 95% prediction interval derived from the controls..C.’s whole–part index of 0.2 fell between the lower (−0.2) andpper limits (0.5) of normal performance.
.3. Discussion
Unlike for faces, configural information facilitated the detec-ion of featural changes in houses. This improvement could not be
sociated mean %error and mean correct RTs with standard error bars (b).
attributed to the mere fact that it was easier to compare one wholestimulus with another regardless of featural arrangement; if thatwere the case then the CPA would have extended to the scram-bled condition. These data therefore provide preliminary evidencefor the idea that R.C.’s perceptual matching deficit is in some waystimulus specific.
One might argue that the house stimuli in Experiment 4 weresimpler than the face stimuli in Experiment 3, and that accordingly,R.C. would have shown a face CPA if the face stimuli were of a com-parable form (i.e. line drawings instead of digitized photographs).However, if his poor matching ability was determined by stimuluscomplexity then his performance should have been similar acrossthe upright and inverted conditions of Experiment 1 in which stim-ulus complexity was equated. Second, we re-analyzed the patterns
of RT and error obtained from the control groups of Experiments 3and 4 to establish if they were either slower or less accurate in anyexperimental conditions of the face CPA experiment compared tothe house CPA experiment. No significant differences were foundin either the RT or accuracy data (all F ratios < 4.0), which suggests
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710 D. Wilkinson et al. / Neurop
hat the distinction seen in R.C. did not reflect the fact that the facetimuli were naturally harder to judge than the house stimuli.
. General discussion
This study set out to investigate the source of deficit in an indi-idual who, following right-sided stroke, is profoundly unable toecognise faces. Consistent with other prosopagnosics with uni-ateral right hemisphere damage, R.C.s problem involves a failureo apprehend the configural properties of faces. This conclusion isased on the fact that he failed to show either a normal inversionffect (Experiment 1) or configural superiority effect (Experiment) for faces. Unlike previous cases, however, his configural deficitoes not simply enforce a greater reliance on part-based analysis.ather, it actually compromises this process; the discrimination of
ace parts was at chance when familiar configural cues were presentsee Experiment 1) yet greatly improved when familiar configuralues were diminished through inversion, scrambling (Experiment) or masking (Experiment 2). While this kind of impairment haseen observed in patients who have suffered damage to both cere-ral hemispheres, we are unaware of its presentation followingnilateral damage.
What do the current observations tell us about how the right andeft cerebral hemispheres process faces? First, they provide sup-ort for two prevailing views: (1) the fact that R.C. cannot matchhole, upright, normally arranged faces supports the view that the
ight hemisphere is needed for configural/holistic processing (e.g.hodes, 1993), and (2) the fact that R.C. is sensitive to the identityf face parts when these are presented outside a familiar config-ral arrangement supports the view that the left hemisphere can,t least under certain conditions, sustain decisions about face partshen the right is damaged (e.g. Barton et al., 2002).
The data permit other, perhaps more interesting, inferencesbout the capacity of R.C.’s left hemisphere to match face parts.n one hand, his failure to apprehend normally configured facearts could reflect a pre-morbid inability. That is, his left hemi-phere might never have been able to do this, and had always reliedo a greater or lesser extent on processes in the right hemispherehich following stroke became dysfunctional. Against this idea are
he facts that split-brain patients appear equally able to judge theamiliarity of face parts when responding with either their right oreft hand (see Keenan, Wheeler, Platek, Lardi, & Lassonde, 2003), andhat greater neural activity is commonly seen in the left comparedo right hemispheres of healthy controls when matching face partsRossion et al., 2000). Alternatively, R.C.’s failure to recover localnformation could reflect the fact that his left hemisphere can actu-lly recover local information from whole upright faces, but thathis ability has been compromised by negative interference fromamaged processes in the right hemisphere. With regard to this
atter account, while the facilitatory effects of inter-hemisphericransmission following brain damage are well documented (seerooks, Wong, & Robertson, 2005) there are far fewer reports ofne hemisphere inhibiting the other, not least within the realm oface processing.
What kind of configural deficit could give rise to this failureo access face parts? Several authors have alluded to a perceptualnterference between separate featural and configural processingtreams in which the specific formation of part-based represen-ations is somehow compromised when configural processes aretrongly engaged (e.g. de Gelder & Rouw, 2000a, 2000b; Boutson
Humphreys, 2002). This account can explain why R.C. could not
atch face parts when presented in the normal configuration, but
eeds refining before it can also explain why he was able to matchormally configured house parts so well. Though not the focus of theresent study, this kind of dissociation could emerge if houses and
aces are encoded within different processing streams (e.g. Yovel &
logia 47 (2009) 1701–1711
Kaniwisher, 2004), each with its own configural processor. If truethen R.C. could have sustained damage to configural processes inthe ‘face stream’ but not the ‘object stream’. Another interpretationis that house and face stimuli are encoded by configural processesthat reside within a single, common processing stream, but thatthe two forms of stimuli place different demands on these con-figural processes. If true then it is conceivable that R.C. sustaineda lesion that led to the same configural processes being able torecover information from houses but not faces. To accept this lat-ter interpretation one would, however, have to reconcile the factsthat the processing demands for houses and faces were consider-ably different as to generate a configural superiority effect for onestimulus but not the other in the patient, yet considerably similaras to generate comparable configural superiority effects for bothstimuli in the controls.
A final issue concerns the role that R.C.’s hemi-spatial neglectcould have played in shaping the results. We were very careful todesign our experiments so that the effects of any lateralized spatialbias would be minimized (see Section 2). Perhaps more convinc-ingly, it is difficult to see how any leftward sensory/attentionalloss could account for the observed improvements in R.C.’s facematching performance because this was achieved while the lateralpositions of face images were held constant. However, neglect isalso associated with non-lateralised forms of visual impairment,one of which concerns the ability to switch attention betweenthe global and local levels of hierarchically organised visual forms(Lamb, Robertson, & Knight, 1989; Robertson, Lamb, & Knight,1988). As was the case in our patient, individuals who suffer fromthis form of impairment typically show damage to superior tempo-ral/inferior parietal areas of the brain.
Such a problem in hierarchical switching would likely hamperthe perception of both faces and objects. In line with this, R.C.’smatching times were elevated for both stimulus types, and hisvisual search times for visual feature conjunctions were abnormallyslow (see Section 2). However, one can imagine that his face match-ing would be especially affected by a switching deficit. Normativestudies show that attention is typically drawn to the configural,as opposed to local, level of faces which in healthy individuals isbeneficial because it orients processing towards aspects of the facethat often allow fast and efficient individuation (see Maurer, Grand,& Mondloch, 2002). Given that R.C. cannot apprehend configuralinformation, this bias would however be detrimental and wouldnecessitate a switch to the local level before faces could be individ-uated. Regrettably, if R.C. was poor at making this switch then hewould be doubly disadvantaged when trying to recognize faces; notonly would he be unable to apprehend their configural attributes,but he would also find it difficult to re-orient attention towardsthose local elements that had been successfully encoded. In thecase of objects, while this switching deficit would slow the rateat which structural descriptions could be formed, R.C. might notshow the same double-disadvantage because he can make use ofboth configural and local attributes.3
If R.C. really does find it difficult to move attention between hier-archical levels then he might be better at discriminating face (andobject) parts when attention is pre-cued to the featural as opposedto global level. Both Barton et al. (2002) and Joubert et al. (2003)
3 We should point here out that while a switching deficit might affect judgmentsfor faces more than objects, it cannot easily explain why configural informationfacilitates decisions about houses yet impairs those about faces. It merely providesanother reason why his face matching is so poor.
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o longer had to be divided across multiple features simultane-usly.
In conclusion, we confirm that damage to the right hemispheres sufficient to impair the configural apprehension of faces. We havelso shown, for the first time, that this configural deficit can hinderhe apprehension of face parts when these are presented in theiranonical, everyday arrangement (e.g. within whole, upright facesn which the features are normally arranged). This may highlightn additional reason why patients who present with right unilat-ral lesions are likely to suffer from prosopagnosia. The study alsoighlights circumstances in which the left hemisphere cannot sup-ort local judgments, however, at the present time we cannot sayhether this is a pre-morbid characteristic or the result of right-
ided stroke. Lastly, we point out the difficulty in making broadereneralisations from single-case studies. Patient R.C. has a veryarge lesion that was sustained over 20 years ago, and also suffersrom hemi-spatial neglect. We must be careful in assuming thatis pattern of performance reflects how other brains work, and asconsequence, we emphasise the need to conduct similar studiesith other individuals who are afflicted with prosopagnosia.
cknowledgements
We thank Isabel Gauthier and Nick Donnelly for their commentsn an earlier version of the manuscript, and are grateful to Kristineundgren for referring the patient. This work was supported in party Merit Review Grants to William Milberg and Regina McGlincheyrom VA Medical Research and VA Rehabilitation Research andevelopment.
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