Face recognition by brain-injured patients: A dissociable ability?

Neuropsychologia,

FACE

1970, Vol. 8, pp. 395 to 402. Pergamon Press.Printedin England

RECOGNITION BY BRAIN-INJURED A DISSOCIABLE ABILITY ?*

PATIENTS:

ROBERT K. YIN Department

of Psychology, Massachusetts

Institute of Technology, Cambridge, Massachusetts,

U.S.A.

(Received 3 February 1970)

Abstract-Patients with right posterior cerebral injuries did more poorly than patients with other unilateral injuries and normal control subjects in recognizing different faces. When the faces were presented upside-down, however, those with the other unilateral injuries did worse than the right posterior group and the normal controls. This dissociation between upright and inverted presentations was not found with pictures of another common object, houses of similar architecture. The results support the notion that, among the disorders caused by

right posterior injuries, there does exist a material-specific deficit in recognizing faces. BY ANY objective measure, human faces are highly similar, yet people have little difficulty in distinguishing one face from another, and in remembering many faces for long periods of time. GALTON [I] was perhaps the first to note this paradox of easy differentiation in spite of great objective similarity. Neither he nor others since his time, however, have tried to explain the origin of this ability. One possibility is that people are especially endowed to remember faces; individual identification based on the face might play a special biological role, similar to that played by voice identification, for instance, in some species of birds [2]. Recognizing faces would thus involve a predisposition for interpreting the distinctive features of the face, but not necessarily relate to the ability to recognize other common objects. Another possibility would be that face recognition forms one aspect of the more general ability to distinguish and remember different visual objects. The relative ease in recognizing faces would reflect the vast amount of experience people have normally had in looking at faces, but would not call upon skills differing from those used in remembering other objects. The examination of brain-injured patients presents a unique opportunity to compare these two possibilities. Basically, if certain injuries selectively impair face, but not object recognition, then there would be some reason to believe that face recognition might be a special ability. Conversely, if face and object recognition were always impaired by the same injury, then the opposite conclusion would be reached. But establishing whether a recognition deficit is face-specific is not as easy as it might first appear to be. To begin with, a rare syndrome in which patients report being unable, on the basis of facial cues alone, to recognize persons highly familiar to them, has been knownever since such a case was first reported by CHARCOT [3]. BODAMER [4] labeled this deficit ‘prosopagnosia’ in order to indicate his belief that a face-specific process, more primitive than that

* This study was supported by NIH Clinical Research Center Grant FR-88 to M.I.T., and by grants to Professor H.-L. Teuber from the John A. Hartford Foundation, Inc., New York, N.Y. and the National Institute of Mental Health, MH-05673. The author wishes to thank H.-L. Teuber for his continued advice and encouragement throughout all phases of the study. 395

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ROBERTK. YIN

used for recognizing other objects, had been disrupted. Several others, however, have countered that the deficit is not peculiar to faces, but forms part of a more general deficit in visual recognition; they cite the other disorders shown by these patients, such as the inability to distinguish one chair from another, as evidence for a more general deficit [e.g. _?,5, 61. Unfortunately, patients with prosopagnosia do exhibit complex arrays of symptoms and do appear with such low incidence that no conclusive analysis of the face deficit has been possible. In spite of several reports of new cases [e.g. 7-1 I], the extent to which the deficit may be material-specific, i.e. li_mited to faces, has not been determined. In recent years, more sensitive face-recognition tests have been designed, and administered to larger groups of patients, not just those who spontaneously complain of difficulties in recognition. This has resulted in the consistent finding that patients with right posterior cerebral injuries have difficulty in recognizing faces, doing more poorly than patients with left hemisphere injuries or normal control subjects [12-141. However, the more sensitive recognition tests have mainly used unfamiliar faces, exposed only during the test situation. Since prosopagnosia most prominently involves a failure to recognize well-known faces, the degree to which the right posterior deficit is related to cases of prosopagnosia is difficult to determine. Direct attempts to test the relationship have led to different results. DERENZI et al. [ll] showed that a patient with prosopagnosia did extremely poorly on a battery of face recognition tests using unknown faces. Recently, however, H~?CEANand TZAVAKAS [15] reported that one of their patients with a 17-year history of prosopagnosia performed normally on a variety of face-matching tests. In an indirect attempt to assess the possible relationship, WAKKINGTON and JAMES [16] compared recognition for famous faces with recognition for unfamiliar ones. Although patients with right posterior lesions did worse on both, no correlation between the two tests was found; but this result could have been attributed to the procedural differences between the two tests. Nevertheless, the question of whether the deficit in recognizing unfamiliar faces is facespecific is still highly pertinent. Only DERENZI and SPINNLER [12], however, have directly They found that right posterior injuries, but not compared face and object recognition. other unilateral ones, impaired performance on three different recognition tests, which used faces, abstract figures, and chairs, respectively. But performance on the chair test was only mildly impaired, and did not correlate with performance on the other two tests. Since the faces thus seemed to have been treated more like abstract figures than chairs, the authors concluded that the difficulty in recognizing faces reflected a general difficulty The different scores on the three tests, however, could in making subtle discriminations. have reflected differences in the difficulty of the tasks alone, and further clarification is therefore needed. Determining the material-specificity of a recognition deficit requires at least two tests, alike in procedure, yet using different materials for recognition. If a deficit is materialspecific, then one type of brain injury should impair performance on one of these tests, but not the other, and a second type of brain injury should have the reverse effect. The combined results would be strong evidence that the mechanisms underlying performance on the two tests were actually different as indicated by what TEUBER has called “double dissociation of symptoms” [17, 181. In this way, for instance, MILNEK and KILMURA [19] showed that left, but not right temporal-lobe injuries disturbed recognition of easily verbalized, visual materials, while right, but not left temporal-lobe injuries disturbed recognition of not easily verbalized, visual materials.

FACE RECOGNITION

BY BRAIN-INJURED PATIENTS: A DISSOCIABLE ABILITY?

397

However, even if a face recognition deficit were established in this manner, its materialFor instance, faces are so familiar and may specific nature could still be questioned. require such subtle discriminations that few comparable tests of object recognition exist; any demonstrable deficit in recognizing faces would not necessarily be material-specific, but could very well be a result of the differential levels of familiarity or discriminability. One way of trying to avoid the dilemma is to use two face tasks, involving similar materials and procedures, but testing face recognition under two different conditions. Clear dissociation of results on such tasks would reduce the weight of arguments based on familiarity or discriminability. Recently, experiments with normal adult subjects have provided two such face tasks [20]. In these experiments, face recognition was compared with recognition for three other classes of familiar objects, which were like faces in being customarily seen in one orientation: photos of houses, airplane silhouette drawings, and cartoon stick figures. The performance of normal adults was tested under two conditions: when all pictures were upright, and when all were inverted. Inverting the pictures made all materials more difficult to recognize. Face recognition, however, was disproportionately impaired by inversion; although the faces were easier to remember than the other materials in the upright condition, they were harder to remember in the inverted condition. In addition, analysis of the individual differences among the subjects showed an interesting effect: although all subjects had greater difficulty with inverted than upright faces, those who did better in remembering upright faces tended to be the ones who did especially poorly in remembering inverted faces, while those who did worse for upright faces tended to do better than others for inverted faces. Such a negative correlation between upright and inverted tasks was not found on tests for the other materials, where subjects who did better in the upright condition also did better in the inverted condition. These results suggested that faces were different from the other materials. Some facespecific process, perhaps, made the recognition of upright faces easy, but was of little use in the recognition of all other materials, including the inverted faces. Furthermore, the upright and inverted recognition tests represented two face tests which met the requirements for testing brain-injured patients. To support the notion of a face-specific process, two hypotheses were suggested regarding the performance of brain-injured patients: (1) right posterior injuries, which presumably lead to poorer recognition of normally presented, i.e. upright faces than other unilateral injuries, should also lead to less impairment on inverted face recognition; and (2) such a relationship, if found for face recognition, should not hold for the recognition of other familiar, complex, and meaningful materials customarily seen in one orientation.

METHOD 1. Subjects This study was part of a broader survey of the long-term effects of brain injury, still in progress as a joint enterprise of the Shattuck Hospital (Harvard Medical School) and the M.I.T. Psychology Department. A nationwide roster of men with open or closed head injuries incurred in the Korean conflict had been established by Colonel Arnold Meirowsky for Army personnel and by Lt. Commander William Caveness for Navy personnel, both of whom had originally seen many of the patients in Korea. The current addresses of these men were obtained by the National Research Council, and all of those who could be located were visited by field workers of the American Red Cross. The men examined at Harvard and M.I.T. include all those on the roster who live in eight states of the Northeastern United States: Maine, Vermont, New Hampshire, Massachusetts, Rhode Island, Connecticut, New York, and Pennsylvania.

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The subjects in the present study represented the first 68 consecutive admissions in the Harvard-hJ.1.T. survey, and these included 37 patients who had sustained some loss of brain substance, proven by history of missile penetration through scalp, skull and dura into the brain, this fact being corroborated by surgical records obtained during debridement of the brain wound and by roentgenographic evidence secured during the course of the survey; 19 patients with closed head injuries sustained in combat, and followed by briefer or longer periods of unconsciousness; and 12 normal control subjects, who served in the same military units as the brain-injured men, but who themselves had suffered no central nervous system disease or damage during the Korean conflict. The 37 patients with penetrating wounds were divided into five categories: patients with bilateral injuries, i.e. those who had evident loss of tissue in both hemispheres; patients with unilateral (left or right) frontal injuries, i.e. those who had missile penetrations of the frontal bone but no known injuries eleswhere; and patients with unilateral (left or right) injuries anywhere else, i.e. non-frontal areas. Table 1 summarizes the number of patients in these five categories the number with closed head injuries, and the number of normal control subjects.

Table I

1. Summary

Penetrating Bilateral Frontal Left Right Posterior Left Right Total,

2.

Closed

3.

Normal

of brain-injured

injuries: 13 3 3 (parietal,

temporal,

or occipital) 7 II

Penetrating

head injuries control Total,

cases

subjects

All cases

37 19 12 68

2. Materials The materials were the same as those used in a previous study [ZO]. They consisted of 64 different picall black and white, for each of two types of objects: photographs of faces and of houses. The faces were studio portraits of adult males, chosen to be similar with respect to general age, expression, and lack of outstanding distinguishing features, such as glasses, beards, or unique marks. All poses were full face, and the pictures were trimmed just under the chin of each face to eliminate as much clothing as possible. The houses were generally of the same architecture, but were not as uniform as the faces in orientation of view or size of picture. In addition, since all were actual photographs, the pictures included trees and other natural features, although they were trimmed to minimize the presence of distinguishing features such as fences, front stoops, and roof markings. All pictures were mounted on 3 x 5 in. cards for presentation. The pictures were randomly divided into two mixed sets, each set havin, e equal numbers of faces and houses. Each set had an inspection series of 20 faces and 20 houses, and a test series of I2 pairs of faces and 12 pairs of houses. The pairs contained one old picture (an exact duplicate of a picture in the inspection series) and one new picture (one not previously shown). Since only 24 pairs were in the test series, there were 16 pictures in the inspection series which did not recur in the test series. The order of presentation of the 40 inspection-series pictures was randomized, with the two exceptions that neither of the two materials was shown for more than four consecutive cards, and that there were always at least two of the nonrecurring pictures, one of each type of material, at either end of the series. The order of the 24 test series pairs was dictated by the order of pictures in the inspection series, so that there was a constant lag between each inspection picture and its occurrence in the test series. Finally, the use of the two sets was alternated, so that half of the patients saw one set rightside-up, and the other set upside-down. and the other half of the patients had the sets reversed. tures,

FACE

RECOGNITION

BY BRAIN-INJURED

PATIENTS:

A DISSOCIABLE

399

ABILITY?

3. Procedure

Each patient was tested individually. He first viewed one set of materials rightside-up, looking at the inspection series of 40 pictures, presented singly and turned by Eat a rate of 3 set per picture. Then the test series, consisting of the 24 pairs, was presented, also rightside-up. For each pair, the patient had merely to indicate which picture was the old one, i.e. the one he had just seen in the inspection series. The patient proceeded at his own rate in the test series. The patient then went through the same procedure with the other set of materials, except that the whole set was presented upside-down. All patients and control subjects were thus tested for recognition memory for four conditions, viewing both faces and houses in both upright and inverted orientations. Since all were tested on the upright orientation before the inverted one, the order of presentation between these two conditions was not actually balanced. However, the previous study had shown that the order did not affect the results [20].

RESULTS Table 2 shows the mean errors for the upright and inverted presentation for the five categories of penetrating injuries, the patients with closed head injuries, and the normal control subjects. For purposes of analyzing the cases of unilateral penetrating injury, the patients with an injury on the left side or a right frontal injury were treated as a group, and those with right posterior injuries as a second group. This division was followed because of the desire to compare performance by the right posterior cases, those with all other unilateral injuries, and the normal control subjects. The data from the bilateral and closed injury groups, though reported, were not used in any further analyses. Table 2. Mean errors (Sixchance

performance) Presentation

Subject Group Faces

Upright Houses

Faces

Inverted Houses

1. Penetrating injuries: Bilateral Frontal Left Right Posterior (parietal, temporal, or occipital) Left Right

2.92

3.17

4.85

4.54

1.67 1.33

2.67 2.33

6.00 5.00

3.67 1.33

1.57 2.82

3.14 3.00

6.43 3.82

4.29 4.73

2.

Closed head injuries

1.74

2.68

3.90

3.05

3.

Normal controls

1.25

2.67

4.58

3.83

Focusing on the performance of the right posterior, other unilateral, and normal control groups on the two face tests, an analysis of variance showed that there were significant differences as a function of the two tests, F(1,66)=34.02, p-cO.0005, and of the tests X subject group interaction, F(2,66) = 3.82, p < 0.05, but not of the subject groups, F(2,66) < 1. The significant difference between the two tests reflected the fact that inverted faces were consistently more difficult to remember than upright faces. More important, however, was that the tests X subject group interaction was significant. Further analysis showed that this was because the right posterior group did more poorly than the patients with other unilateral injuries, t(22) = 3.78, p ~0.002, two-tailed, and the normal controls, t(21) = 3.19,

ROBERT K. YIN

400

~~0.01, two-tailed, on the upright face test; but the patients with the other unilateral injuries did worse than the right posterior group, t(22) =2.87, p
n

z

Houses

Normal control (NE121

Rlght p05tWOr IN=ll)

Other unIlater(ll (N’l3)

Subject

(N=l31

Closed head (N’l91

(N=131

head iN-I91

Bilateral

group

Inverted 6 t

l-l

Normal

Control IN=121

Right posterior (N=lll

0ttW unilateral (N=l31

Subject

group

FIG. 1.

DISCUSSION The results have shown that injuries to the right posterior cerebral area produced a deficit in recognizing upright faces which was not exhibited by patients with other unilateral injuries or by normal control subjects. That this deficiency was specific to face recognition

FACERECOGNITIONBY BRAIN-INJUREDPATIENTS: A DISSOCIABLE ABILITY?

401

indicated first by a dissociation between the upright-face test and another test using the same materials and procedure, except that the faces were presented upside-down. On that test, the patients with right posterior injuries did better than the patients with other unilateral injuries. Secondly, comparable testing with another type of material, pictures of different houses of the same architecture, did not affect performance in the same way as had the face tests. Further exploration of the face recognition deficit would seem to have to deal with the dissociation between upright-face and inverted-face recognition : the upright face has some characteristics which the inverted face apparently lacks. However, whether such characteristics are indeed unique to faces, or whether they may be shared to some extent by other visual patterns, is not clear. On the one hand, if face recognition requires a special type of visual scanning, or an appreciation for objects with certain symmetries, then other visual patterns might also have these characteristics, and inversion could have a similar effect on the recognition of such patterns. In the light of this possibility, it may be important to note some very recent experiments by H~CAEN and TZAVARAS [15]. They compared the ability to match face pictures with the ability to match pictures of several other types of objects, and found that right posterior injuries severely impaired performance on the face tests, but only slightly or not at all on the other tests. Their tests did not depend upon inverting the pictures, and yet they reached similar conclusions regarding the potentially special role played by faces. On the other hand, if face recognition involves appreciation of the face as a social object, and memory for the people represented by the face, then the characteristics might very well be unique to faces, By this interpretation, the difficulty in looking at upside-down faces results mainly from the inability to discern the “expression” of the face or some other attribute relating to the face as a social object; patients with right posterior injuries were unable to appreciate fully such attributes in the first place, perhaps treating faces as other types of non-human objects, and were consequently less affected by inversion, i.e. the difference between their scores for upright and inverted face recognition were smaller than those for the other groups. In summary, the present data indicate that a general impairment in distinguishing and remembering visual objects does not account for the impairment shown by patients with right posterior lesions on tests of face recognition. Rather, they suggest that attention should be focused on the special characteristics of the face, and in particular to those characteristics which the upright face does not share with the inverted face, for a full explanation of the face recognition deficit. was

REFERENCES 1. GALTON, F. Inquiries into Human Faculty and its Development, p. 4. MacMiljan, New York, 1883. 2. THORPE, W. H. Perceptual basis for group organization in social vertebrates, especially birds. Nature 220, 124-128, 1968. 3. HBCAEN, H. and ANGELERGUES,R. Agnosia for faces (prosopagnosia). Archs Neural. 7, 92-100, 1962. 4. BODAMER, J. Die Prosop-Agnosie. Arch. Psychiat. Nerv. 179, 6-53, 1947. 5. BAY, E. Disturbances of visual perception and their examination. Brain 76, 515-550, 1953. 6. CRITCHLEY, M. The Parieta/ Lobes, pp. 291-8. Hafner, New York, 1953. 7. BEYN, E. S. and KNYAZEVA, G. R. The problem of prosopagnosia. J. Neural. Neurosurg. Psychiat. 25 154-158, 1962. 8. COLE, M. and PEREZ-CRUET, J. Prosopagnosia. Neuropsychologia 2, 237-246, 1964. 9. GLONING, I., GLONING, K., HOFF, H. and TSCI-IABITSCHER, H. Zur Prosopagnosie. Neuropsychologiu 4, 113-132, 1966.

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10. GLONING, K. and QUATEMBER, R. Method&her Beitrag zur Untersuchung der Prosopagnosie. Nerrropsychologia 4, 133-141, 1966. 11. DERENZI, E., FAGLIONI, P. and SPINNLER, H. The performance of patients with unilateral brain damage on face recognition tasks. Cortex 4, 17-34, 1968. 12. DERENZI, E. and SPINNLER, H. Facial recognition in brain-damaged patients. Ne~crology 16, 145- 152, 1966. in facial recognition in patients with cerebral 13. BENTON, A. L. and VAN ALLEN, M. W. Impairment disease. Cortex 4, 344-358, 1968. and recall after right temporal-lobe excision in man. Neuropsychologiu 14. MILNER, B. Visual recognition 6, 191-209, 1968. 1969. 15. HBCAEN, H. and TZAVARAS, A. Personal communication, investigation of facial recognition in patients 16. WARRINGTON, E. K. and JAMES, M. An experimental with unilateral cerebral lesions. Cortex 3, 317-326, 1967. 17. TEUBER, H.-L. Physiological psychology. Ann. Rev. Psycho/. 6, 267-296, 1955. of perception and memory in man: Reflections on methods. 18. MILNER, B. and TEUBER, H.-L. Alteration In Analysis qf Behavioral Change, L. WEISKRANTZ (Editor), pp. 268-375. Harper & Row, New York, 1968. visual learning defects after unilateral temporal lobectomy 19. MILNER, B. and KIMURA, D. Dissociable in man. Paper read at 35th ann. meeting, Eastern Psychol. Assoc., Philadelphia, April, 1964. faces. J. exp. Psychol. 81, 141-145, 1969. 20. YIN, R. K. Looking at upside-down RCsumC-Dans une Bpreuve de reconnaissance de visages, les performances des malades avec atteinte cCrCbrale postkrieure droite ttaient infkrieurcs d celles des malades avec autre atteinte unilattrale et g celles des sujets du groupe de contrble. Lorsque les visages etaient prtsentCs en position inverste, les malades avec autre atteinte unilatirale etaient infkrieurs au groupe postCrieur droit et aux sujets de contrble. Cette dissociation entre les prtsentations normales et inversees n’6tait pas retrouvCe avec des reprCsentations d’autres objet familiers, tels que des maisons d’architecture similaire. Ces rCsultats sont en faveur de l’existence, parmi les dCsordres dtterminCs par les l&ions postbieures droites, d’un dkficit spCcifique quant au matCrie1 prtsentB pour la reconnaissance des visages. Zusammenfassung-Patienten mit rechtsoccipitalen Verletzungen haben griirjere Schwierigkeiten beim Unterscheiden von Gesichtsziigen als Kranke mit anderen halbseitigen VerWenn man dagegen Gesichter auf dem Kopf stehend letzungen und als Kontrollpersonen. darbot, boten andere halbseitig Verletzte schlechtere Leitstungen als rechts hinten Verletzte und Normalpersonen. Dieses Auseinanderfallen zwischen aufrecht und umgedreht gezeigten Objekten wurde bei Bildern und anderen gelgutigen Objekten, wie z.B. Hlusern und sonstigen Bauwerken, nicht festgestellt. Diese Resultate erlauben die Folgerung, daR unter den St& rungssyndromen rechtsoccipitaler HirnschCden sich ein Sttirungssymptom findet, das ausschlieplich das Gesichtserkennen betrifft.