Neuroprvchologu. Vol. 20. No. 5. pp. SIS-511. 1982 Pnnted I” Great Bntam.

0X8-3931 8~.OsOSlSO7SO3CO~O Pcrgamon Press Lrd.

FACE RECOGNITION BY MONKEYS: ABSENCE OF AN INVERSION EFFECT

CHARLES BRUCE*

Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health. Bethesda, MD 20205. U.S.A.

(Receiced 24 February 1982)

Abstract-The effect of inversion of faces upon learning visual discriminations by macaque monkeys was studied with simultaneous discriminations, concurrent discriminations, and transfer tests. In no case was performance with upright stimuli superior to that with inverted stimuli; that is, there was no obvious inversion effect. Studies of human face recognition indicate that the inversion effect is mediated by an orientation-dependent face recognition mechanism that matures within the right hemisphere during childhood. Absence of an inversion effect would indicate that monkeys may not have such a mechanism. 11 was hypothesized that the macaque’s relatively precocious development. smaller cortex, and lack of hemispheric specialization may preclude the maturation of such a mechanism.

HUMANS are especially adept at face perception. Faces are our primary means of identifying each other, and the average person has a prodigious capacity for remembering and discriminating faces. Furthermore, the perception of facial expressions is an important channel of social communication.

Much of this aptitude to analyze and remember faces is lost if faces are upside down. Not only are familiar faces difficult to recognize when inverted, but unfamiliar inverted faces are more difficult to learn to recognize than upright unfamiliar faces. This inversion effect is an important research tool. For example, it has been utilized to dissociate deficits in face recognition from general impairments in object recognition. YIN [l] tested patients with lesions of the posterior right hemisphere and found that recognition of previously unfamiliar upright faces was more severely affected than the recognition of inverted faces; in fact, some of these patients showed no inversion effect. Because upright and inverted faces are equivalent with respect to color, size, symmetry and comptexity, Yin’s result indicates that these patients’ deficit involved processing specific for upright faces, in addition to more general visual disorders often associated with right hemisphere damage [2].

Not only are inverted faces a particularly good control for aspects of face perception research, but the lateralization, development and loss of man’s special aptitude for recognizing faces parallel that of the inversion effect. When stimuli are confined to one hemisphere of normal right-handed adults, via tachistoscopic presentation, only the right hemisphere, which is superior to the left in face recognition, shows the inversion effect [3]. Young children do not show an inversion effect for face recognition; however, the

*Please address requests for reprints to Charles Bruce, National Institutes of Health, Bldg 36, Rm l-D-18, Bethesda, MD 20205, U.S.A.

515

516 CHARLES BRLCE

development of adult-like performance of facial recognition coincides with the emergence of differential processing of upright and inverted faces [4, 51. Thus across different lines of

research the inversion effect is closely associated with man’s special aptitude to recognize faces.

The present study sought to determine if the inversion of faces would impair the ability of

macaque monkeys to learn to recognize them. Macaque monkeys are nearly identical to man on a variety of basic psychophysical measures: acuity, spectral sensitivity, wavelength discrimination, color categorization, critical flicker frequency, orientation anisotropy, etc. [6-S]. Furthermore, the face plays an important role in identification and communication in

most primate societies. Therefore it seemed plausible that the similarities in visual performance between man and monkey might extend to this sophisticated perceptual

process and that macaques would show an inversion effect for faces. Experimental evidence bearing on this aspect of face perception in the monkey is inconclusive. OVERMAN and DOTY

[9] report that their monkeys found inverted faces “more difficult to recognize when seen

upside down”,* whereas ROSENFELD and VAN HOESEN [IO] report their monkeys “not confused by manipulations in orientation” of faces. The inversion manipulation was not the

primary focus in either of these studies, and neither was designed to determine if monkeys have an inversion effect for faces similar to the effect found in man. The results of the present study indicate that monkeys do not.

METHODS

Subjects

The subjects were six experimentally naive male cynomolgus monkeys (Macacafascicularis) weighing 2.8-3.5 kg.

Appararus

The monkeys were trained in a sound-insulated box. Two rear-projection screens (11.0 x 8.5 cm) were located 16.5 cm apart along one wall of the box, and a tray to hold the food pellets (300 mg banana-flavored monkey chow, Noyes) was located midway between the screens. A clear plexiglass panel in front of each screen was hinged on microswitches, and the monkeys responded by pressing these panels. The discriminanda were projected onto the screens by Industrial Electronic Engineers Series 80 readout units. Stimulus presentation and reinforcement were programmed automatically, and errors were automatically tallied.

Color slides of 16 other laboratory monkeys, also male Macacajiscicularis, were projected for stimuli. Most were full-face, front-illuminated portraits. When projected the faces filled the screens and were about two-thirds of life- size.

Procedure

The monkeys were food deprived and trained for 100 trials per day, 7 days a week. On each problem they were trained until a criterion of 90 correct trials in a single IOO-trial session was attained.

*The present findings are not at variance with those of Overman and Doty. Face inversion was not the principal manipulation in their study, and was not balanced across the tasks. To summarize, monkeys were trained to match- to-sample a particular set of human and monkey faces. Following two consecutive days of meeting a 90% criterion and an additional day of training, ali with the same set of upright faces, the monkeys were tested for one day with all stimuli (samples and matches) inverted. Average performance declined from 91% to 82”j, correct (estimates from Fig. 3), but it is unknown whether a similar decline would occur ifmonkeys were first trained with inverted faces and then tested once with upright ones. For example, although the monkeys initially learned the match-to-sample paradigm with slides of miscellaneous objects, they required further training to meet criteria with upright faces. It was not reported how well the monkeys performed when first tested with upright faces or how many days oftraining with upright faces were needed. Therefore, although the experiment shows that monkeys are af/ected by the orientation of the face stimuli, in the absence of a balanced design it does not demonstrate an intrinsic superiority for recognition of upright faces.

FACE RECOGSITIOV BY MOSKEYS: ABSESCI OF A\i l>bERSIOV EFFECT 517

At the end of the 7-see intertrtal interval, the overhead light was turned off and the discriminanda were projected on the screens. A response to the panels during the intertrta! interval reset the interval. A response during the trial turned off the stimuli and turned on the overhead light. A response to the positive stimulus was rewarded, and a response to the negative stimulus was counted as an error. The sequence of positive stimulus positions was randomized. To acquaint the subjects with the apparatus and the simultaneous discrimination paradigm. all subjects first learned three preliminary problems not involving faces.

Exprrimental design

All monkeys completed eight problems involving faces in the same order. For each monkey all stimuli of four problems were upright and all stimuli of the other four problems were inverted. The same face was positive in each problem. whether the problem was upright or inverted. For three monkeys problems I. 3.5 and 7 were given with inverted stimuli and for the other three monkeys problems 2.4.6 and 8 were given with inverted stimuli. Thus the orientation variable was balanced across both problems and monkeys.

Each problem was composed of slides of a unique pair of monkeys. Problems 1 and 2 were simple simultaneous discriminations: problems 3-8 had two parts, a learning part and a transfer part. Once the subject had learned the simultaneous discrimination involving a new pair offaces to criterion. the transfer part of the problem was begun on the next day. The transfer stimuli were five additional pairs ofslides ofthe faces used in the learning part, but differing from them in expression, size and lighting. The transfer procedure was a concurrent discrimination paradigm: each of the five pairs was presented 20 times per session, and the order was random under the constraint that each pair appear 10 times (five with the correct face on the left and five with it on the right) within every 50-trial block. The transfer testing was continued until the 90% criterion was again obtained, that is. until the subject was responding consistently to the new views of the same monkey that was rewarded during the learning part of the problem. For problems 3 and 4, the learning part, as well as the transfer part, was a S-pair concurrent discrimination.

RESULTS

Learning

There was no significant effect of face inversion upon the learning phase of the experiment. Table 1 contains the total errors to criterion for each problem and subject. Inspection of this table shows that both across problems and across monkeys there was considerable overlap between the scores on upright and inverted faces. Based on one-tailed Mann-Whitney CJ tests, the orientation manipulation did not have a significant effect at the 0.05 level of confidence on the learning phase of any of the eight problems taken individually across

monkeys or on any of the six monkeys considered across problems. The sources of learning errors were also estimated with a three-factor analysis-of-variance, the factors being stimulus orientation (two levels), problem (eight levels), and subject (six levels). The subject and problem factors were both highly significant [F(5, 34)= 14.4; F(7, 34)=9.7] and together accounted for 69% of the variance in the error scores. The orientation factor was not

significant [F( 1, 34) = 1.43; in fact, the mean learning errors for upright (57 errors) and inverted (60 errors) faces were nearly the same.

Table 1. Total errors during learning phase (inverted problems underlined)

Problem

Subject 1 2 3* 4+ 5 6 7 8

Thyme 44 15 23 23 34 17 14 3 Nutmeg 216 65 113 ;T;i 92 54 23 1

Oregano 68 )I( 40 a 80 22 8 D

Astair I14 64 ss 74 26 7 16 Karloff 97

22

46 91 75 3s

Bogart 174 90 47 35

80 136 100 241 - 21 - B 33

*Concurrent problems.

51s CH*RLES BRCCE

The average number of errors on the initial day of the problems was only slightly better than chance (41.2). and there was no overall effect of orientation upon this initial performance (42 errors for upright vs 40.4 for inverted). There was. however. considerable variation in performance at the beginning of problems. including instances where the initial performance svas significantly worse than chance. For example, one monkey began problem 6 with 30 consecutive responses directed at the incorrect face of the pair. These predispositions towards the incorrect stimulus (or away from the correct one) were most apparent at the beginning of two particular problems (5 and 6) and occurred in instances of

both upright and inverted presentations of these two problems. The cause may have been a similarity between the appearance of monkeys in these and previous problems. Conversely, there were four occasions when the 900/;, criterion was met on the first day of a problem. This happened twice on problem 7 and twice on problem 8. apparently reflecting an overall tendency for the monkeys to improve over problems.

In summary. the learning of the simultaneous discriminations was clearly affected by individual aptitude, problem difficulty. cumulative experience with the paradigm, and predispositions towards the stimuli. These factors appeared to account for much of the variability of the error scores in Table 1. In contrast. the orientation of the stimuli in the problems had no significant effect on the learning performance.

The monkeys appeared to recognize the additional photographs of the faces in the transfer part of the experiment. and the orientation of the faces had no significant effect upon their performance. Table 2 shows the errors on the first day of transfer. On 12 occasions, six involving upright faces and six involving inverted faces, the 90”,, criterion was met on the first day. For every problem there was an overlap between the scores of the three subjects learning the problem with upright faces and the three subjects havin, 0 the faces inverted; therefore orientation did not have a significant effect on transfer on any of the six problems taken individually. again based on one-tailed Mann-Whitney L’ tests. Similarly. there was no significant effect of orientation upon the transfer performance of any individual monkey. Overall, the mean number correct on the first day was 82.4 for the inverted problems and 82.0 for the upright problems; an analysis-of-variance showed that whereas the subject and

problem factors were both highly significant, the orientation factor was not. Although responses to correct stimuli were differentially rewarded during the transfer

parts ofthe experiment, it appeared that the scores on the first day were largely unaffected by this contingency; comparisons between the initial and final 50 trials on the first day revealed

Table 2. Per cent correct on first day of transfer phase (inverted problems undsr!medl

Problem Subject 3 4 5 6 7 8

Thyme 93 93 57 56 80 98 Nutmeg 85 89 98 91 43 90

Oregano 91 91 78 79 71 ss

.A.stalr 65 94 93 ii 74 94 Karloff G 90 7R 77 60 96 Bogart z 91 iFi 69 - 5i 67

only minor improvements. In general, the errors during the transfer task were largely

confined to one or two of the five pairs of stimuli used, and were fairly persistent. For example, one monkey made errors on all 20 presentations of a particular stimulus pair for three consecutive days.

In summary, the monkeys appeared to recognize immediately most of the transfer slides whether the slides were upright or inverted, and the variability in the error scores appeared to be largely the results of variations in subject aptitude and the difficulty of the individual transfer stimuli.

DISCUSSION

It is somewhat surprising that the inversion of faces, which usually has a robust effect upon human performance, had no significant effect upon the monkeys’ performance in this experiment. Macaque monkeys and humans are members of the same order, both have highly developed visual systems with nearly identical basic visual abilities, and for both species faces and facial expressions play an important role in social interactions. Given the present results, however, species differences must be emphasized.

Rather than consider all species differences, both established and suspected, that could conceivably affect the present results, I would like to focus on a general explanation based on what is known about the development, lateralization and neurology of face recognition in humans. Children under the age of 10 remember photographs of faces presented upside down about as well as they do those presented upright. CAREY and DIAMWD [4] suggest that the subsequent emergence of an inversion effect around age 10 yr reflects the maturation of an

efficient but orientation-specific, configurational representation of faces. This representation is apparently lateralized since the right-hemisphere advantage for faces also emerges at the same time [S]. only the right hemisphere shows the inversion effect [3] and face recognition deficits, including loss of the inversion effect, are more often associated with damage to the

right than to the left hemisphere [l, 1 l-131. These facts indicate that the right hemisphere contains the face recognition system that

operates in a configurational or Gestalt manner, which is congruent with the generally holistic manner of right-hemisphere function. Faces can still be recognized in the absence of this configurational system, but presumably in a different and less efficient manner. Children, prior to the maturation of this system, certainly recognize faces, but their method is characterized as “piecemeal” by CAREY and DIA,MOXD [4]. Facial stimuli confined to the left hemisphere by tachistoscopic presentations are also recognized, albeit less quickly than when confined to the right hemisphere [ 143. Furthermore, the patients with face discrimination difficulties described in neurological studies can still recognize familiar faces and learn to recognize new faces. True prosopagnosia, a striking inability to recognize even familiar faces, appears to have a different anatomical basis from the more common discrimination deficits. BENTON [ 1 I] suggests that true prosopagnosia may require bilateral damage, whereas the discrimination difficulties are found in many patients with lesions confined to one (usually the right) hemisphere.

Since the configurational face recognition system is strongly associated, both ex- perimentally and logically, with the face inversion effect, the result of the present study suggests that macaque monkeys lack this orientation-specificconfigurational mechanism for face recognition. There are several related differences between man and monkey which could explain why the monkey lacks such a mechanism. First, the infancy of macaque monkeys

520 CHUXLES BRUCE

lasts only 1.5 yr, and they are fully mature adults following an additional 6 yr of a juvenile

phase [lj]. Perhaps this precocity precludes the development of a configurational mechanism for face recognition, which, as indicated earlier, requires 10 yr in humans. Second, unlike humans, monkeys appear to have minimal hemispheric specialization for any function [ 161. including face recognition [9]. Finally, this orientation-specific configur- ational face recognition mechanism could be the domain ofcortical areas present in man but absent in the monkey. The human cortical mantle has an expanse several times that of the macaque, and part of this increase must represent further differentiation of visual association cortex.

These explanations of why the monkey lacks the orientation-specific configurational specialization for face recognition found in man are clearly less compelling in the case of the great apes. The apes have longer developmental stages than monkeys, and their cortical expanse is more comparable to man’s than the monkey’s is. Furthermore, although no functional hemispheric specializations have been demonstrated in the apes, there are, as in the human, consistent anatomical asymmetries in the cerebral cortex [17]. Apes have not been tested for the face inversion effect, but the constructive behavior ofchimps [18] suggests that they may possess orientation-specific face schema.

In summary, the present experiment indicates that. for the macaque monkey, face inversion has little effect on visual performance. In light of the parallels of the inversion effect with the development, lateralization, and loss of man’s special aptitude for face recognition, the absence of an inversion effect in monkeys implies that they have a qualitatively different mechanism of face recognition. In particular, it suggests that monkeys may lack the orientation-specific, configtirational, face recognition mechanism that is located within the

right hemisphere of adult humans.

Acknowledgements-Support for this work was provided by NSF Grant ENS-75-23634 and NIH Grant MH-19420 to Charles Gross and by NIH Postdoctoral Fellowship NSOS804 to Charles Bruce. The assistance of Charles Gross in all aspects of this study is gratefully acknowledged.

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REFERENCES

YIN, R. K. Face-recognition by brain-injured patients: A dissociable ability? Nrtrropsycha/ogiaS, 395402, 1970. MILNEH, B. Visual recognition and recall after right temporal lobe excisions in man. Neuropsgchologia 6, 191-209, 1968. LEEHEY, S.. CAREY. S.. DIAXIOND, R. and CAHN, A. Upright and inverted faces: The right hemisphere knows rhe difference. Corrrx 14, 411419, 1978. CAKEY, S. and DIAMOSD. R. From piecemeal to configuration representation of faces. Science 195, 312-313, 1977. DIAI~OND, R. and CAKEY. S. Developmental changes in the representation of faces. J. exp. Child Psycho/. 23, I-22, 1977. BOLTZ. R. L., HARWERTH, R. S. and S~IITH, E. L. Orientation anisotropy of visual stimuh in rhesus monkey: a behavioral study. Science 205, 5 I I-5 13. 1979. DE VALOIS. R. L. Central mechanisms of color vision. In Handbook ojSensory Physiology. R. Jung (Editor), Vol. 7/3A. Springer-Verlag. Berlin, 1973. SANIXLL. J., GROSS, C. G. and BORSTF.I\. M. H. Color categories in Macaques. J. camp. physiol. Psycho/. 93,

626435, 1979. OVERMAN. W. H. and DOTY, R. W. Hemispheric specialization displayed by man but not macaques for analysis of faces. Neuropsychologia 20, I 13-128. ROSEZFELI). S. A. and V.*N HOESEN, G. W. Face recognition in the rhesus monkey. Neuropsychologia 17, 503-509, 1979. BF.NTON. A. L. The neuropsychology of facial recognition. Am. Psycho!. 35, 176-186, 1980. H~XAEN. H. and ANGELERCUES, R. Agnosia for faces (prosopagnosia). Archs Neural. 7,92-100. 1962.

FACE RECOGNITION BY .UONKEYS: ABSENCE OF IV ISVERSION EFFECT 521

13. MEADOWS. J. C. The anatomical basis of prosopagnosia. J. New-o/. Nrurosur. Psychiar. 37, 489-501. 1974. 14. R~ZZOLATTL G., UWLT~. C. and BERLL.CCHI, G. Opposite superiorities of the right and left cerebral hemispheres

in discrimination reaction to physiognomic and alphabetical material. Brain 94, 43 1442, 1971. 15. JOLLY, A. The E~;oIctrion OJ Primate Behacior. Macmillan, New York, 1972. 16. HAWLTON, C. R. and TIEW,N, S. B. Cerebral dominance in monkeys? Neurops_vchologia 12, 193-197, 1974. 17. LE~IAY, M. and GESCHWIND. N. Hemispheric differences in the brains of Great Apes. Brain Behac. Euol. 11.

48-52, 1975. 18. PREXKK, D. Putting a face together. Science 188, 228-236, 1975.

RESUME

C'effet de l'inversfon de physfonomies SW l'ap- prentissage de discriminations visuelles par 4es macaques a et6 itudi6 dans des tithes de discrfminations simultanies ou concurfentes et de transfer? de discrimination. Dans aucun cas la performance avec le stimulus tcte en haut ne s'est r&Slie supkieure i celle avec le stimulus inversi. 11 n'y avait done pas d'effet d'inversion evident. Les etudes de reconnaissance des visages chez l'honm indiquent que l'effet d'inversion est dJ i un mkanisme de reconnaissance des visages sensible d l'orientatfon, dont la maturation se prodult dans l'h6misphPre droit au COWS de l'enfance. L'absence d'effet d'inversion in- dique que les singes pourralent ne pas possider un tel m&a- nisme. cln a fait l'hypothke que le &veloppement relativement prkoce des macaques: leur cortex mains itendu et leur absence de spkialisation hemisphirique pourralent s'opposer i la ma- turation de ce mkanism.

Zusammenfassung: ----

Der Effekt einer Umkehrung van Gesichtern auf das Erlernen van

visuellen Diskriminationen wurde bei Makaken mit simultanen Diskriminationen.

konkurrierenden Diskriminationen und Transferaufgaben iiberpriift. In keinem

Falle war die Leistung mit aufrechten Stimuli der Leistung mit umgekehrten

Stimuli iiberiegen. Das heist: es gab keinen offensichtlichen Inversionseffekt.

Untersuchungen des menschlichen Gesichterkennens zeigen, da13 der Inversions-

effekt iiber einen orientierungsabh~ngigen Gesichtserkennungsmechanismus

vermittelt wird. der in der rechten Hemisphare wlhrend der Kindheit reift.

Abwesenheit eines solchen Inversionseffektes wilrde anzeigen, dal.3 die Affen

solch einen Mechanismus nicht besitzen. Es wrde die Hypothese formuliert,

dal.7 die verhlltnismlflig rasche Entwicklung des Makaken, sein kleinerer

Kortex und der Mange1 an hemisphsrischer Spezialisation die Reifung eines

solchen Mechanismus verhindern kiinne.