The Neuropsychology of Face Perception and Facial
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THE NEUROPSYCHOLOGYof
FACE PERCEPTIONand
FACIAL EXPRESSION
edited by
Raymond Bruyer
University of Louvain
Psychology Press
Taylor & Francis Group
NEW YORK A N D L O N D O N
First Pub]ished]986 by
LawrenceErlbaum Associates,[oc., Publishers
Published2014 by PsychologyPress
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LIbrary of Congrns Cataloging·ln·Publication Dala
Main entry under titl e:
The Neuropsychologyof face perceplionand facial
expression.
Includes bibliographiesand index.
l. Neuropsychology . 2. Face perception. 3. Facial
expression. I. Bruyer, Raymond. iDNLM : 1, Face-
pllysiology. 2. Facial Expression. 3. Neuropsychology.
WE 705 N494)
QP360.N495 1986 612'.82 85·27420
ISBN 978-0-898-59602- 1 (hbk)
Publi sher's NOle
The publisherhasgoneto greatlengthsto ensurethe quality
Mlh is reprint but pointsoulthat someimperfections in the
original may be apparent.
List of Contributors
Raymond Bruyer • University of Louvain
Ruth Campbell· University of Oxford
Isabelle Clerc • University of Rouen
Antonio R. Damasio • University of Iowa Hospitals and Clinics
Hanna Damasio • University of Iowa Hospitals and Clinics
Jules B. Davidoff· University College of Swansea
Haydn D. Ellis· University ofAberdeen
Pierre Feyereisen• Universityof Louvain
Robert G. Ley· Simon Fraser University
Luigi Pizzamiglio • University of Rome
Phyllis Ross-Kossak• New York University Medical Center
Justine Sergent·McGill University
Esther Strauss· University of Victoria
Guy Tiberghien· University of Grenoble
Gerald Turkewitz • Hunter College of the City of New York
Andrew W. Young· University of Lancaster
Pierluigi Zoccolotti • University of Rome
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Contents
Preface xi
Foreword xv
Chapter 1 Introduction:ProcessesUnderlying FaceRecognition
Haydn D. Ellis 1
Introduction 2
PerceptualProcesses 4
FaceRegister 7
Long-Term SemanticStore 14
Overview 22
PART I: BRAIN DAMAGE AND FACE PERCEPTION
Chapter 2 The Anatomical Substrateof Prosopagnosia
AntonioR. Damasioand Hanna Damasio 31
Conclusion 36
Chapter 3 The Cognitive Locus of Prosopagnosia
Guy Tiberghien and Isabelle Clerc 39
Familiarity, Context,and Prosopagnosia:
The Caseof A. H. 40
Toward a Cognitive Theory of the Agnosia of Faces 47
Conclusion 56
vii
viii CONTENTS
Chapter 4 FaceProcessingand Brain Damage:Group Studies
RaymondBruyer 63
Memory 6,4
From Memory to Perception 72
Discrimination 75
Discussionand Conclusion 82
PART II: LATERAL DIFFERENCESFOR FACE
PERCEPTIONIN NORMAL SUBJECTS
Chapter 5 MethodologicalConstraintson Neuropsychological
Studiesof FacePerceptionin Normals
JustineSergent 91
Introduction 91
MethodologicalConsiderations 93
Conclusion 117
Chapter 6 A Micro and Macrodevelopmental View of the Nature
of Changesin ComplexInformation Processing:
A Considerationof Changesin Hemispheric
AdvantageDuring Familiarization
Phyllis Ross-Kossakand Gerald Turkewitz 125
Chapter 7 The Specificity of FacePerception:Evidencefrom
PsychologicalInvestigations
J. B. Davidoff 147
Innateness 148
NeurologicalConsiderations 149
Theoriesof FaceRecognition 151
RecognitionAbility 152
Recognitionof Faces:Featuresand Configurations 154
Recognitionof Faces:Mechanismsand Mental
Representations 157
Conclusion 162
Chapter 8 SubjectCharacteristicsin Lateral Differencesfor Face
Processingby Normals:Age
AndrewW. Young 167
Studiesof the Developmentof Lateral Asymmetriesfor
FaceProcessing 168
CONTENTS ix
How the Resultsof Studiesof the Developmentof Lateral
Asymmetriesfor FaceProcessingRelate to Wider
Issues 184
Overview and Conclusions 192
Chapter 9 Lateral Differencesin FaceProcessing:Effects of Sex
and Cognitive Style
Pierluigi Zoccolotti and Luigi Pizzamiglio 201
Introduction 201
Individual Differencesin FacePerception:Effect of Sex 203
Sex Differencesin Laterality of Facial Recognition 204
Field Dependence-Independence and Face Perception 206
Field Dependence-Independence and Laterality of Face
Perception 209
Relative Contribution of Sex and Field Dependencein
FacePerception 212
PART III: NEUROPSYCHOLOGYOF FACIAL EXPRESSION
Chapter 10 Productionand Comprehensionof EmotionalFacial
Expressionsin Brain-DamagedSubjects
Pierre Feyereisen 221
The Expressionof Emotion by Facial Movements 222
The Laterality Issue:Right and Left HemisphereLesions
Compared 230
Conclusions 239
Chapter 11 Asymmetriesof Facial Action: SomeFactsand Fancies
of Normal FaceMovement
Ruth Campbell .247
Are FaceAction AsymmetriesReal? 247
Pulling Faceson Command 248
The NeuroanatomicalBasis for Asymmetric Facial
Actions 252
HemisphericSpecializationand HemifaceAction 256
Chapter 12 HemisphericAsymmetriesin the Perceptionof Facial
Expressionsby Normals
RobertG. Ley and Esther Strauss 269
HemisphericAsymmetriesand EmotionalValence 270
ExpressionDetection 278
Judgmentof Degreeand Direction of Emotionality 280
X CONTENTS
Are the Processorsfor Facial ExpressionsUnique? 281
Summary 286
Author Index 291
Subject Index 305
Preface
Obviously, the face is an important stimulus both ecologically and psychoso-
cially. An illustration of this importancecan be found in the "face-ism" phe-
nomenon:the headinvolvesonly 15-20%ofthe total body, but people(especially
men) are generally depictedby meansof an impressiveoverstatementof their
face (see, e.g., Archer, lritani, Kimes, & Barrios, 1983). The face, as a psy-
chological stimulus, supportstwo main functions: It is the main sourceof infor-
mation for discrimination and identification of people, and it constitutesthe
structuralgroundof many nonverbalmessages,including information about the
emotional state of the person (for a similar view, see Ellis, 1983). Due to the
importanceof the face, a great number of studies in experimentalpsychology
have been conducteddating back to the very outset of the scientific study of
behavior and cognitive events. An overview of the field can be found in the
book edited by Davies, Ellis, and Shepherd(1981).
This tradition in experimentalpsychology, togetherwith early observations
concerningdefectsof face recognitionafter brain damageand with the increasing
developmentof neuropsychology,has generated,in the last 2 decades,a great
number of neuropsychologicalinvestigationsconcerningthe visual processing
of faces and, more recently, the mechanismsof facial expressionand the per-
ceptionof facial expressions.Classically,and in function of their own viewpoint
concerningthe relationshipsbetweencognitive eventsand cerebralmechanisms,
authors consider that natural (pathological) or experimentaldissociationsevi-
dencedin neuropsychologycan contribute to a better understandingof cerebral
mechanismsand of functional differencesbetweencerebralregions(in this "neu-
roscientific" view, cognitive dissociationsrepresentone way among others of
studyingthe brain) or to a betterexplanationof cognitive mechanismspermitting
xi
xii PREFACE
hypothesesabout postulatedprocessesto be tested (in this "cognitivist" view,
cerebralpropertiesare one way amongothersof studyingcognition). Both points
of view are representedin this book.
The neuropsychologyof face processinghas developed,logically and chron-
ologically, in threesuccessiveperiods,the commencement of eachperiod being
associatednot with the end but with the renewalof the precedingone. This kind
of evolutiori-in neuropsychology,however, is not unique for the study of the
processingof faces. The first period was characterizedby reports of isolated
casessuffering from a defectin the recognitionof familiar faces. This approach
datesback for more than a century and reacheda high point in the publication
of Bodamer(1947), who proposedthe term prosopagnosiafor this pathological
condition. It continuesin the light of the findings of the other two approaches.
The second series of studies grew out of the first. Since 1966 (De Renzi &
Spinnler, 1966), neuropsychologistshave given groups of brain-damagedsub-
jects to various testsof faces discrimination andrecognition,the subjectsbeing
selectedonly on the basis of lesion localization, thus not specifically as proso-
pagnosic. New, unfamiliar faces were generally employed. The aim of such
studies, as was usual in the 60s, was to searchfor deficiencies(dissociations)
in the mechanismsof faceprocessingandto establishcorrelationswith anatomical
localizationsandespeciallylesion1ateralization.Accordingto the usualevolution
in the field, the third period, starting in 1971 (Geffen, Bradshaw,& Wallace,
1971; Rizzolatti, Umilta, & Berlucchi, 1971), was characterizedby the partic-
ipation of normal subjectsin experimentsusing lateralizedtachistoscopicpres-
entationsof the material. It was assumedthat the performancewould differ in
function of the stimulatedhemifield, due to the specific mode of processingof
the contralateralhemisphere(given the crossedorganizationof the visual neu-
ronal pathways).
In spite of the amount of empirical data so far collected, and recent books
devotedto the right cerebral hemisphere (Perecman, 1983; Young, 1983), no
book has yet beenpublishedconcerningthe neuropsychologyof face perception
and facial expression(at leastin English: seeBruyer, 1983). To our knowledge,
there are only reviews of empirical data and/or critical and theoreticalpapers,
generally limited to particular aspectsof the field (Benton, 1980; Blanc-Garin,
1984; Damasio, Damasio,& Van Hoesen,1982; Davidoff, 1982; Ellis, 1975,
1983; Hay & Young, 1982; Hecaen,1981; Jeeves,1984; Meadows,1974; Rinn,
1984;Sergent& Bindra, 1981; seealsothe specialissueof HumanNeurobiology,
1984,3). The presentbook is an attemptto fill this lacune. It could be that this
absenceis due at least partially to a lack of firm theoreticalfoundation for the
neuropsychologicalapproachto the mechanismsof face processingand to meth-
odologicaldifficulties. Thereare, indeed,controversiesconcerningthe inferential
processtoward cerebralasymmetriesfrom observedlateral differencesas well
as very weak explanatorypower: The "theories"are mainly descriptivesystems,
not models permitting operationalizationand predictions. Note again that this
PREFACE xiii
kind of limitation in neuropsychologyis not specific to the field surveyedin the
presentbook. On the other hand, someimportant gains have beenmadeduring
the last decadeand it may be that an earlier publication would have beenpre-
mature. Indeed, up to about 1974 it was well establishedthat the processingof
faces was a right-brain competencewhereasmore recent empirical data have
revealedthat this asymmetryhad to be qualified carefully by characteristicsof
the input, of the subjects,and of the cognitiverequirementsof the task. As noted
by Ellis (1983), "If researchon cerebral asymmetry in processingfaces had
stoppedin the early-to-mid 1970s, we would probably all happily acceptthat
the right hemisphereis better adaptedfor processingcomplex patterns,such as
faces. ( ... ) However, researchdid not stop" (p. 38).
Therefore, the presentbook has been designednot to build a coherentand
powerful neuropsychological"theory" of face processing.Neuropsychologyis
still a young scientific field, and the first real theory remainsto be elaborated,
the main effort beingdevotedto theproductionof empiricaldata.The contributors
thus try to presentthe readerwith a completeoverview of the publisheddata,
togetherwith hypothesesand methodologicalcritical comments,about variables
that have beenshown to be important. I would like to thank thesecontributors
for their collaboration as well as Harry Whitaker and the editorial board of
LawrenceErlbaum Associatesfor their fruitful support in this venture.
For the Introduction, Ellis has taken on a hazardoustask: He lists the main
theoreticalproblemsin face processingfrom a cognitive point of view. Then, a
series of chaptersis devoted to reviews concerning neuropsychologicaldata
related to face perception, offered by pathological observations(Part I) and
studiesof lateral differencesin normal subjects(Part II). The chaptersby Dama-
sio and Damasio(anatomy), and Tiberghien and Clerc (mechanisms),on pro-
sopagnosia,and Bruyer, on the processingof faces after brain damage, are
followed by contributionsconcerningthe analysisof lateral differencesin normal
subjects:methodologicalconsiderations(Sergent),familiarity effects(Ross-Kos-
sak and Turkewitz), the question of specificity (Davidoff), and the effects of
subjectscharacteristics(Young-age;Zoccolotti and Pizzamiglio-sexand cog-
nitive style). The third part of the book deals with the non-verbal messages
conveyedby the face: Feyereisenreviewsdataissuedfrom brain-injuredsubjects
and Campbell (expressions)and Ley with Strauss(perceptionof expressions)
survey the data producedby normal subjects.
RaymondBruyer
REFERENCES
Archer, D., lritani, B., Kimes, D. D., & Barrios, M. (1983). Face-ism:five studiesof sexdifferences
in facial prominence.Journal of Personalityand Social Psychology,45, 725-735.
Benton, A. L. (1980). The neuropsychologyof facial recognition.AmericanPsychologist,35, 176--
186.
xiv PREFACE
Blanc-Garin,J. (1984). Perceptiondes visageset reconnaissance de la physionomie,dansl'agnosie
des visages.L'anneePsychologique,84, 573-598.
Bodamer,J. (1947). Die Prosop-Agnosie.Archivesfur Psychiatrieund Zeitschriftfur Neurologie,
179, 6--53.
Bruyer, R. (1983). Le visage et l' expressionfaciale: approche neuropsychologique.Bruxelles:
Mardaga. .
Damasio,A. R., Damasio,H., & Van Hoesen,G. W. (1982). Prosopagnosia:anatomicbasis and
behavioralmechanisms.Neurology, 32, 331-341.
Davidoff, J. (1982). Studieswith non-verbalstimuli: In J. G. Beaumont(Ed.), Divided visual field
studiesof cerebral organisation (pp. 29-55). London: Academic Press.
Davies, G., Ellis, H., & Shepherd,J. (Eds.). (1981). Perceivingand rememberingfaces. London:
Academic Press.
De Renzi, E., & Spinnler,H. (1966). Facial recognitionin brain-damagedpatients.An experimental
approach.Neurology, 16, 145-162.
Ellis, H. D. (1975). Recognizingfaces. British Journal of Psychology,66, 409-426.
Ellis, H. D. (1983). The role of the right hemispherein face perception:In A. W. Young (Ed.),
Functions of the right hemisphere(pp. 33-64). London: AcademicPress.
Geffen, G., Bradshaw,J. L., & Wallace, G. (1971). Interhemisphericeffects on reaction time to
verbal and nonverbal visualstimuli. Journal of ExperimentalPsychology,87, 415-422.
Hay, D. C., & Young, A. W. (1982). The human face: In A. W. Ellis (Ed.), Normality and
pathologyin cognitivefunctions (pp. 173-202). New York: Academic Press.
Hecaen,H. (1981). The neuropsychologyof face recognition:In G. Davies,H. Ellis, & J. Shepherd
(Eds.), Perceivingand rememberingfaces (pp. 39-54). London: Academic Press.
Jeeves,M. A. (1984). The historical roots and recurring issueson neurobiologicalstudiesof face
perception.Human Neurobiology, 3, 191-196.
Meadows,J. C. (1974). The anatomicalbasisof prosopagnosia.Journal ofNeurology,Neurosurgery,
and Psychiatry, 37, 489-501.
Perecman,E. (Ed.). (1983): Cognitive processingin the right hemisphere.New York: Academic
Press.
Rinn, W. E. (1984). The neuropsychologyof facial expression:a review of the neurologicaland
psychologicalmechanismsfor producingfacial expressions.PsychologicalBulletin, 95, 52-77.
Rizzolatti, G., Umiita, c., & Berlucchi, G. (1971). Opposite superioritiesof the right and left
cerebralhemispheresin discriminativereactiontime to physiognomicaland alphabeticalmaterial.
Brain, 94, 431-442.
Sergent, J., & Bindra, D. (1981). Differential hemisphericprocessingof faces: methodological
considerationsand reinterpretation.PsychologicalBulletin, 89, 541-554.
Young, A. W. (Ed.). (1983). Functionsof the right cerebral hemisphere.London: AcademicPress.
Foreword:
From Patchwork to
Melting Pot
PATCHWORK
For psychologists,this book may seem incomplete. Indeed, some important
topics related to face processingare not consideredhere. Three partially inter-
related areasof researchcome to mind in particular: animal studies, psycho-
pathology, and self-recognition.Actually, psychopathologyand animal studies
are only marginally relevantto humanneuropsychology,and very few data are
available concerningrecognition of one's own face and animal studies. These
data are briefly reviewed in the first part of this Foreword. First, we examine
the visual processingof one'sown face (neuropsychologicaldata, animals,psy-
chopathology), and then we discuss the other studies concerning the visual
processingof faces (animals and psychopathology).
Visual Recognition of One's Own Face
The visual recognitionof one'sown face (seethe readingscollectedby Mounoud
& Vinter, 1981) is mainly studiedin developmentalpsychology.It is generally
claimed(but seethe critical review of Anderson,1984a)that the true recognition
of oneself follows a period during which the stimulus seen in the mirror is
consideredto be anotherperson(for empirical dataand reviews seeAmsterdam,
1972; Boulanger-Balleyguier,1964, 1967; Brunet & L6zine, 1949; Wallon,
1959;Zazzo, 1948, 1975, 1977a,1977b).The studyof BeardsworthandBuckner
(1981), nevertheless,shows that the recognition of oneselfby adults is easier
kinestheticallythan visually. Moreover(but seethe critical commentsof Ander-
son, 1984b), in an evolutionist perspective,it seemsthat animals are unable to
xv
xvi FOREWORD
reachthis stageof true self-recognition,with chimpanzeesbeing a major excep-
tion (for data and reviews, see Anderson, 1983; Boulanger-Balleyguier,1968;
Gallup, 1968, 1970, 1977; Gallup, McClure, Hill, & Bundy, 1971; Hall, 1962;
MacLean, 1964; Premack,1975; Zazzo, 1979). Somedataalso are availablein
the field of non-neuropsychological behavioraldisturbances(psychiatry). First,
we note that somepsychiatrichallucinatorysyndromesare characterizedby the
continuousvision of oneselfin the visual field (heautoscopie)or, conversely,
by an absenceof imagewhen looking in a mirror (Zazzo, 1948). Second,social
behaviorwithout self-recognitionhas beendescribedwhen early dementedpatients
(in a psychiatric sense)were presentedwith a mirror (Abely, 1930; Delmas,
1929). Third, and againsta common intuitive notion, Neumanand Hill (1978)
haveshownthat autisticchildrenwereableto recognizethemselvesin a videotape
mirror image. Fourth and finally, social behavior without self-recognitionhas
been describedfor mentally retardedchildren (Shentoub,Soulairac, & Rustin,
1954; Soulairac,Shentoub,& Rustin, 1954) and Vinter, Mounoud, and Husain
(1983) have shown by meansof a distorting mirror that mentally retardedadults
had a distordedself-image.
Somedata are more relatedto neuropsychologicalproblematics.It has been
shownthat the level of deficiency of self-recognitionin a mirror can be an index
of severity of cognitive impairment in senile dementedpatients(Ajuriaguerra,
Strejilevitch, & Tissot, 1963; Postel, 1968). A deficiency in self-recognition
also has been noted in Korsakoff patients (Michel, 1978). Prosopagnosicsare
frequently reported as having difficulties in recognizing themselvesin mirror
images (examples:Bauer, 1984; Bodamer, 1947, CasesI & 2; Bruyer et a!.,
1983; Charcot, 1883; Cogan, 1979, Cases11 & 12; Cohn, Neumann,& Wood,
1977, Case 1; Damasio,Yamada,Damasio,Corbett, & McKee, 1980, Case2;
Michel, 1978; Nardelli et a!., 1982, Case2, Schachter,1976; Shuttleworth,
Syring, & Allen, 1982, Cases1 & 2) or judging their mirror imagesas modified,
strange,or unusual(examples:Bodamer,1947, Cases1 & 2; Bruyeret a!., 1983;
Hecaen,Ajuriaguerra,Magis, & Angelergues,1952; Lhermitte, Chain, Escour-
olle, Ducarne,& Pillon, 1972;Whiteley & Warrington, 1977,Case2). Schachter
(1976) has even describeda caseof prosopagnosialimited to the mirror image
(actually, paroxystical). Finally, it seemsthat split-brain patients are able to
recognizetheir own faces, whateverthe stimulated hemisphereor better with
the right one (Preilowski, 1975, 1979; Sperry, Zaidel, & Zaidel, 1979).
The representationof one's own face is basedmainly on the mirror image;
therefore, in the natural face-to-faceperceptionof peers, the perceivedface is
"reversed"(the right part of the face is seenin the left side of the visual field
and vice versa),but not the face perceivedin a mirror (the right half-faceremains
in the right part of the field). Consequently,dissociationscan be searched
(a) betweenself-perceptionand perceptionof otherfaces,as well as (b) between
self-perceptionin a mirror and self-perceptionon a video TV screen (or on
photographs).This secondkind of dissociationis illustrated by somedemented
FOREWORD xvii
patientswith an adequateself-recognitionin the mirror and no self-recognition
on a video screen(Michel, 1978). As concernsthe first type of dissociation,
there are casesof prosopagnosicpatientsable to recognizethemselvesin pho-
tographsor in a mirror, or for which no mention is madeby authorsconcerning
self-recognition(we incautiously supposeit was preserved);we also note the
study of Mita, Dermer, and Knight (1977), which showedthat peopleprefer the
mirroredto the normal photographof themselves,and the normal to the mirrored
photographof familiars. In a similar line, lateral differencesobservedby Seinen
and Vanderwerff (1969), and Straussand Kaplan (1980), about the emotional
expressionof hemifacesissuedfrom the face of the perceiverhaveto be replicated
and confrontedwith data concerningfaces of other people (see Part III of this
book): the subjectsof the-firstpaperjudgedtheir right hemifaceasmore"positive"
and their left hemifaceas more "negative";thoseof the secondstudy judgedthe
left hemifaceto be more similar to their own mental image of themselveswhen
happinesswas expressed,the right one more similar for sadness,and the left
hemifacemoreexpressivethanthe right for sadness.Finally, Dimond andHarries
(1984) examinedthe use of the hand to touch one'sown face in monkeys,apes
(gorillas, chimpanzees,and orangutans),and humans:the authorsnotedincreas-
ing touching behaviorfrom monkeysto humansand a quasi-similarincreasein
the use of the left-hand (and cross-culturaldifferences in humans; Hatta &
Dimond, 1984); the authorssuggestthat thesedatareflect the evolution of right
hemispheredominancefor the managementof emotionaland non-verbalbehavior.
Face Perception
Regardingface perception,two kinds of information shouldbe mentioned.First,
psychopathologyoffers some observationsconcerningthe processingof faces.
Becauseautism generally is considereda defect of interpersonalinteractions,
autistic childrenhavebeengjven testsof face recognition(e.g., Langdell, 1978).
There are also rare psychiatric syndromes(cf. Enoch, Trethowan, & Barker,
1967) characterizedby "illusions of doubles": the patient is convincedthat the
personseenis in fact someoneelse(Capgras'syndrome),that the sameindividual
is seenwhen two different personsare seen(Fregoli's syndrome),or that various
personsare intermetamorphosed (for theseconditions,seeChristodoulou,1976,
1977). It is being increasinglysuggestedthat such syndromescould result from
a neurologicalpathology involvingthe cerebralhemispheres(Alexander,Stuss,
& Benson,1979;Christodoulou,1976, 1977; Hayman& Abrams, 1977; Luaute,
Bidault, & Thionville, 1978; McCallum, 1973; Merrin & Silberfarb, 1976; Mor-
rison & Tarter, 1984; Waghray, 1978; Weston & Whitlock, 1971). Finally,
Levin and Benton (1977) have shown that the test of Benton and Van Allen
(1968; seeBruyer, this volume) can be usedto discriminatepsychiatricdisorders
from brain disease(seealso Tzavaras,Luaute, & Bidault, 1986).