AN EXPERIMENTAL INVESTIGATION OF FACIAL RECOGNITION IN PATIENTS WITH UNILATERAL

CEREBRAL LESIONS

Elizabeth K. Warrington and Merle James

(The National Hospital, Queen Square, London)

INTRODUCTION

Prosopagnosia, defective recognition of familiar faces, has been described as a distinctive and separate visuo-perceptual defect (Bodamer, 1947; Gentili, Loperfido and Eutizi, 1960; Hecaen and Angelergues, 1962). H~caen and Angelergues found that it was more frequent in cases with right hemisphere lesions than left hemisphere lesions, while, in contrast, object agnosia and colour agnosia are more common with left hemisphere lesions. De Renzi and Spinnler (1966) investigated facial recognition experimentally in a group of un selected patients with unilateral cortical lesions. They found that the right hemisphere group was significantly worse than the left hemisphere group in recognising a previously unknown face from immediate memory, and that performance on the facial recognition test correlated positively with recognition of abstract designs from immediate memory in each group. They considered the hypothesis that the defect in prosopagnosia is the inability to recognise individuality within a given category. However, using a test of recognition of different types of chairs there was no corre­lation with the test of facial recognition, and they concluded that the basic impairment in prosopagnosia is an impairment of subtle discrimination and integration of visuo-perceptive data and not an incapacity for "grasping individuality within a category."

In the present investigation two tests of facial recognition were designed, the recognition of well-known faces and the recognition from immediate memory of what had previously been an unknown face. The aim was to confirm the association of right hemisphere

318 Elizabeth K. Warrington and Merle James

lesions with impairment on tasks requiring facial recognition, and to consider the relationship between recognition of well-known faces and immediate memory for previously unknown faces.

METHOD

Patient Groups

Subjects were selected from patients referred to the Psychology Department for testing. Any patient with good evidence of a unilateral cerebral lesion, able to co-operate in the test situation, and right­handed for writing, was given a preliminary screening test (described in detail by Warrington and James, 1967). The purpose of this test was to exclude in a systematic manner patients with either a severe dysphasia or a severe visual defect.

Sixty-two patients selected in this way were tested. Dr. Gilford, of the radiological department, classified all patients as having frontal, temporal, parietal or occipital lobe lesions, or a combination of these four categories. Patients with lesions involving more than one lobe were included in both groups for comparisons between the lobes of the two hemispheres. Twenty-seven patients had left hemisphere lesions, seven involving more than one lobe. There was clinical evidence of dysphasia in fifteen of these patients. Thirty­five patients had right hemisphere lesions, nine involving more than one lobe. Age, sex, pathology and locus of the lesions are given in Table I.

Ten patients with peripheral nerve lesions were tested as controls. Their mean age was 47, which is comparable to the two experimental groups.

Test Procedure

All patients with cortical lesions were tested on the Wechsler Adult Intelligence Scale. Verbal and Performance I.Q.s were obtained by prorating the scores on four verbal and four performance tests (Arithmetic, Similarities, Digit Span, Vocabulary, Block Design, Picture Completion, Picture Arrangement and Object Assembly).

Recognition of Well-known Faces

Photographs of ten well-known public figures were used: President Kennedy, Mr. Mac Millan, Mr. Kruschev, The Queen, Mr.

Facial recognition and unilateral cerebral lesions 319

TABLE I

Clinical Details of Patient Groups

Left hemisphere patients Right hemisphere patients

Age Sex Aetio- L 2 Dyspha- Age Sex Aetio- Locus2 logy! oeus sia' logy!

1 35 F N T + 1 17 F A T 2 65 M V FPT + 2 53 M N T 3 66 F N P 3 44 F V T 4 57 M V FPT 4 44 F N F 6 39 M N T + 5 60 F N PO 8 38 M A T + 6 46 F N T

10 35 M A P + 7 48 M N TP 11 31 M N P 8 25 F L T 13 33 M N T + 10 41 M V T 14 40 M V PO 11 43 M N P 15 19 F A T 12 43 M N P 16 47 M V FP 13 21 F L T 17 45 M N FP 15 26 F V PT 18 53 F N T 16 25 M A T 19 17 M A P 17 63 M N T 20 60 M N P + 19 37 M N P 21 57 M N T + 21 47 M N P 22 32 M V PO + 22 34 M N PO 23 33 F N T + 23 46 F N T 24 54 M N T + 24 57 M N P 25 30 F V P + 25 31 F L T 30 73 M N T + 26 25 M L T 32 62 F N P 27 52 F N T 33 53 M N T 28 32 M N P 34 31 M L T + 29 42 F L T 35 25 M V FPT + 30 61 F N F 36 38 F N T 32 57 F N FP

33 63 M N P 34 66 M N FP 35 69 F N P 36 59 F N PO 37 46 F V TP 38 62 M V P 39 61 F N PO 40 60 M N P

! A = abscess; N = neoplasm; V = vascular disorder; L = lobectomy. 2 F = frontal; P = parietal; T = temporal; 0 = occipital. , + = presence of dysphasia.

Churchill, Viscount Montgomery, Prince Philip, Jack Hawkins, Kenneth More and Marilyn Monroe. The photographs were 6 x 9 inches, showing the head and shoulders in full view or three-quarter view. The photographs chosen displayed no distinguishing clothing such as uniforms. All patients were shown the photographs in the above order. Patients were asked to name the person, and if

320 Elizabeth K. Warrington and Merle James

they failed to give the correct name they were asked to give any information they could in order to determine whether they had recognised the face. Two types of error were scored; naming errors, when the patient satisfied the examiner that he had, in fact, recog­nised the person by giving other details about him, e. g. profession, country of origin or fame, but could not name him. An error of recognition was recorded when the patient either misrecognised, or was unable to recognise the face.

The ten control subjects with peripheral nerve lesions were tested one and two years later than the patients with cortical lesions.

Immediate Retention of Unknown Faces

The test material consisted of two identical books of photo­graphs, each containing photographs of eight men and eight women, all of whom were unknown to the subjects. The photographs were approximately 4 by 5 inches, and showed only the head and shoulders - little distinctive clothing was present that would aid identification. The patient was shown one of the photographs for ten seconds; he was then given the second set of photographs and required to identify the same face. Eight trials were given, four male faces and four female faces shown alternately. No time limit was set for identification.

This test was given to all the left hemisphere group and thirty­four of the right hemisphere group. The ten control subjects did this test at a later date.

RESULTS

Intelligence Test Results

The mean verbal and performance I.Q.s for the left hemisphere group were 97.5 (range 70-137) and 104.0 (range 69-140) respect­ively. The right hemisphere group had a mean verbal I.Q. of 101.0 (range 82-130) and a mean performance I.Q. of 89 (range 58-117).

Well-known Faces

All incorrect responses on this test were recorded either as an error of naming or an error of recognition. The mean error score for each type of error for each patient group is given in Table II. The right and left hemisphere groups have been sub-divided, and the

Controls Left hemisphere Right hemisphere Left temporal Right temporal Left parietal Right parietal

Facial recognition and unilateral cerebral lesions

TABLE II

Mean Error Scores on Well-known Faces and Immediate Retention of Unknown Faces Tests

Well-known Faces

Naming Errors Recognition Errors

.7 2.5

.91 3.5

.51 1.2 1.2

1.7 .96

2.05 1.19 2.7 1.21 1.62

321

Unknown Faces

.4

.74 1.53 1.0 l.4

.71 l.7

mean error scores for the temporal and parietal groups are also given in Table II. The Mann Whitney U test was used in all group comparisons, and z or U values are given in Table III. The left hemisphere group made significantly more errors of naming than either the control group or right hemisphere group. The left temporal group

TABLE III

Group Comparisons on Tests of Facial Recognition

Well-known Faces Unknown Faces

Naming Errors Recognition Errors

Left hemisphere z = 2.205 z = 1.37 z = 0.08 v. controls p < 0.05 p> 0.05 p> 0.05

Right hemisphere z = 0.53 z = 0.15 z = 2.36 v. controls p > 0.05 p > 0.05 p < 0.05

Left hemisphere z = 2.7 z = 2.33 z == 2.95 v. right hemisphere p < 0.01 P < 0.05 p < 0.01

Left temporal U == 41 U = 80.5 U == 76.5 v. right temporal p < 0.01 P > 0 .05 p > 0.05

Left parietal U == 104.5 U = 98.5 U == 58.5 v. right parietal p > 0 .05 P > 0 .05 P < 0.05

Left temporal v. U == 37 U = 77.5 U == 81.5 left non-temporal p < 0.05 p > 0.05 p > 0 .05

Right temporal v. U = 99 U == 117 U == 141 right non-temporal p > 0.05 p > 0 .05 p > 0.05

Right parietal v. U = 101 U == 132.5 U == 129 right non-parietal p> 0.05 p> 0.05 p> 0.05

322 Elizabeth K. Warrington and Merle James

made significantly more errors of naming than the right temporal and the left non-temporal group, while the left parietal group and the right parietal group are not significantly different.

More errors of recognition were made by the right hemisphere group than the left hemisphere group, and the difference in the mean error scores was significant at the 5% level of probability, but the right hemisphere group was not significantly worse than the control group. However, the control group was tested a year or more later, and it is possible that by this time some of the well­known people were less typical.

Though none of the sub-group comparisons showed any significant differences, the right temporal group had the highest mean score for recognition errors (Figure 1).

KNOWN fACES

RECOGNITION NAMING

~n error score) (Mean error Icore)

Fig. 1

Unknown Faces

The mean error scores for each patient group on this test are given in Table II. The Mann Whitney U test was again used for group comparisons and z or U values are given in Table III. The right hemisphere group is significantly worse than the left hemisphere and control groups on immediate retention of unknown faces (p < .01 and .05, respectively) while the left hemisphere group is not significantly impaired relative to the control group.

Facial recognition and unilateral cerebral lesions 323

The right parietal was significantly worse than the left parietal group (p < .05), but not significantly worse than the remaining right hemisphere cases (Figure 2).

UNKNOWN FACES

2'0 01ean error score)

V')

cr::: 0 ex:: a:::

1'0 w

z « w ~

RH C RT LT RP LP Fig. 2

Correlations between the Faces Tests

Each patient was classified fail or pass according to whether there was at least one error of recognition in the left hemisphere group or two errors of recognition in the right hemisphere group on either the well-known faces or the unknown faces test. The coefficient of concordance between performances on the two tests was calculated ,for the right and the left hemisphere groups separately. There was no significant degree of concordance within either hemisphere group (chF = 0.006 and 0.1 respectively). Though the right hemisphere group made significantly more recognition errors on both these tests than the left hemisphere group, of the 21 right-sided cases to fail on either of these two tests , only 5 failed on both. This failure to find any association between these two tests suggests they are measures of different functions.

324 Elizabeth K. Warrington and Merle James

Association between Visual Field Defects and Facial Recognition Errors

Fifteen of the right hemisphere cases and six of the left hemi­sphere cases had visual field defects. These field defects were restricted to one quadrant in seven of the right hemisphere cases, and in one of the left hemisphere cases. (The thirty-six right hemisphere cases reported by Warrington and James, 1967, included these thirty­five cases.) The median test of significance was used to determine the association of recognition errors and visual field defects in the right hemisphere group. Neither recognition errors on the well-known faces test nor errors on the unknown faces test were significantly associated with visual field defects (chF = 0.2 and 0.91 respectively).

DISCUSSION

In this study the performance of right and left hemisphere groups has been compared on two tests of facial recognition. Previous investigations have shown that right hemisphere groups are impaired relative to left hemisphere groups on tasks involving facial recog­nition. The present study confirms this association of right hemisphere lesions and impairment on tests of facial recognition. The right hemisphere group were impaired relative to the left hemisphere group, both in recognition of well-known faces and in immediate memory for unknown faces.

Comparisons of temporal and parietal sub-groups did not yield any significant results, with the exception of naming errors on the well-known faces test, which were significantly associated with left temporal lesions, and recognition errors on the unknown faces test with right parietal lesions. Nevertheless, inspection of the mean error scores in the parietal and temporal sub-groups is of some inter­est. The right temporal group obtains the highest recognition error score on the well-known faces test, while the right parietal group obtains the highest error score on the unknown faces test. Further­more, the correlation of scores on these two tests was not significant in either the right or the left hemisphere group; in both groups the correlation was very close to zero; in the right hemisphere group the correlation had a negative value. Though these findings cannot be accepted as showing a double dissociation between the right temporal and right parietal lesions on these two types of task, they

Facial recognition and unilateral cerebral lesions 325

do suggest that there may be different functional processes determin­ing them which warrant further investigation in a larger group of patients.

De Renzi and Spinnler's test of facial recognition was very similar to the unknown faces test in the present investigation. They argued that "right brain damage (especially posterior lesions) selectively impairs the high-level integration of vi suo-perceptive data," and that as facial recognition demands a high degree of discrimination between similar visual forms , right hemisphere cases could be expected to show a deficit. Warrington and James (1967) drew attention to the importance of the perceptual complexity in determining a right hemisphere deficit on tasks of visual recognition. They found the right parietal group to be selectively impaired on a variety of visual recognition tasks, including one of immediate memory for simple non-verbal perceptual patterns. In the present study the test of unknown faces, which also demands immediate memory, produced a similar pattern of results (though not reaching significance at the 5% level).

Prosopagnosia, the inability to recognise familiar faces, as an isolated and clear-cut disability, is a rare occurrence in the neurolo­gical literature. The attempt to investigate this syndrome experi­mentally led De Renzi and Spinnler to use the technique of imme­diate recognition of unknown faces - yet in the present study no correlation was found between recognition of well-known faces and unknown faces. If it is accepted that the well-known faces test is more analogous to the clinical entity of prosopagnosia, then it may be argued that the impairment shown on the test of unknown faces is not basic to prosopagnosia.

One may speculate as to whether these findings have any connection with amnesic states which are known to result after bitemporal lobectomy (Scoville and Milner, 1957). It is characteris­tic of amnesic patients that their span of apprehension for both verbal and non-verbal material is relatively intact, while their ability to learn and retain new material and recall any long-term memories is grossly impaired. On this view prosopagnosia could be regarded as a partial amnesia for one category of information, namely, faces, which may be impaired with a right temporal lesion. Further support for this view is to be found in the observation, not yet experimentally verified, that pro sop agnosia and topographical memory loss are frequently observed in conjunction with one another (Beyn and

326 Elizabeth K. Warrington and Merle James

Knyazeva, 1962; Pallis, 1955). There is one common factor linking topographical memory loss (the inability to recognise routes and places) and prosopagnosia; both involve the recognition of a unique visual entity, that is, a particular face or a particular building rather than a mere category. Patients with prosopagnosia are able to recognise a face as a face, and those with topographical memory loss a building as a building, but not which one. It would therefore seem that there may be a long-term memory "store" for visual data within the right hemisphere, which is separately organised from the processing or integration of perceptual data which is necessary for recognition of drawings and immediate memory for faces.

SUMMARY

Sixty-two patients with unilateral cortical lesions were given two tests of facial recognition, which required recognition of well-known faces and recognition from immediate memory of previously unknown faces .

The right hemisphere group was impaired relative to the left hemi­sphere group on both tests. In neither group was there a significant correlation between the scores on the two tasks, indicating that the tasks were tests of separate and distinct functions. The results are discussed in terms of the clinical syndrome, prosopagnosia. It is suggested that prosopagnosia may be a constituent of an amnesic syndrome.

Acknowledgments. We wish to thank the physicians and surgeons of The National Hospital for permission to study and report our findings on patients under their care, and Dr. J. Bull for his co-operation in this investigation. We are grateful to Drs. R. T. C. Pratt and 1. J. Herberg for their advice in the preparation of this manuscript . Our thanks are due to Dr. E . S. Gilford of the Department of Radiology, The National Hospital, for his classification of the radiological data. One of us (M. J.) was supported by a grant from the Medical Research Council.

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