CANADIAN JOURNAL OF PSYCHOLOGY, 1983,37(1), 8-18

Perception of Faces by Patients with

Localized Cortical Excisions*
Bryan Kolb, University of Lethbridge
Brenda Milner and Laughlin Taylor,
Montreal Neurological Institute

ABSTRACT Patients with various unilateral lesions and normal subjects

were given a face-perception task. Two composite symmetrical faces
were made by combining the left or right half of a normal face with its corre-
sponding mirror image, the subject indicating which composite more close-
ly resembled the original face. Regardless of upright or inverted orientation,
normal subjects and patients with left-hemisphere lesions exhibited a
preference for the left-visual-field composite. Patients with right posterior
lesions failed to show a bias in either orientation. Right temporal and
parieto-occipital cortex appear to contribute to facial perception, regard-
less of orientation.

RESUME Une tache de perception de visage est presentee a des patients

atteints de lesions unilaterales variees ainsi qu'a des sujets normaux.
Deux visages symetriques sont constitues en combinant la partie gauche
ou droite d'un visage normal avec son image en miroir correspondante.
Les sujets doivent indiquer lequel des deux visages ressemble le plus a I'o-
riginal. Les resultats indiquent qu'independamment de I'orientation droite
ou inversee, les sujets normaux et les patients atteints de lesions a I'hemis-
phere gauche montrent une preference pour I'element present dans le
champs visuel gauche. Les patients souffrant de lesions posterieures
droites ne presentent pas ce biais. II semble done que le cortex temporal
et parieto occipital droit contribue a la perception du visage et ce, indepen-
damment de I'orientation.

Faces convey a wealth of social and affective information to people. The

importance of accurate perception of faces and facial expression has thus
led to considerable interest in the neurological mechanisms underlying the
processing of faces. Although little is known about the details of neurologi-
cal organization, there is general concensus that the right hemisphere plays
a dominant role in facial recognition. Within the clinical literature distur-
bances of facial recognition and memory have been most often associated
with right posterior lesions (Benton & Van Allen, 1968; Meadows, 1974;
Milner, 1968, 1980; Newcombe, 1973; de Renzi, Faglioni, & Spinnler, 1968;

'This research was supported by the Medical Research Council of Canada Grant MT2624 to
Brenda Milner and a Natural Sciences and Engineering Research Council of Canada Grant to
Bryan Kolb. We are grateful to Dr. Theodore Rasmussen, Dr. William Feindel and their associ-
ates at the Montreal Neurological Hospital for the opportunity to study their patients. Address
reprint requests to Bryan Kolb, Department of Psychology, The University of Lethbridge, Leth-
bridge, Alberta, Canada.

8
 Perception of faces 9

Warrington & James, 1967a; Yin, 1970). Similarly, tachistoscopic studies

of normal subjects have shown a left visual field advantage for the recogni-
tion of faces, regardless of whether the behavioural measure is reaction
time (Geffen, Bradshaw, & Wallace, 1971; Rizzolatti, Umilta, & Berlucchi,
1971; St. John, 1981; Strauss & Moscovitch, 1981; Suberi & McKeever,
1977) or recognition accuracy (Hilliard, 1973; Klein, Moscovitch, & Vigna,
1976; Leehy, Carey, Diamond, & Cahn, 1978). Further evidence of the spe-
cialized role of the right hemisphere in facial perception comes from the fol-
lowing: studies of the perception of chimeric faces after cerebral com-
missurotomy (Levy, Trevarthen, & Sperry, 1972); studies demonstrating a
left visual field bias in judgements of photographs under unrestricted view-
ing conditions (Campbell, 1978; Gilbert & Bakan, 1973; Lawson, 1978);
and studies showing a right-hemisphere dominance for the perception of
emotional expression in faces (Buchtel, Campari, de Risio, & Rota, 1978;
DeKosky, Heilman, Bowers, & Valenstein, 1980; Hansch & Pirozzolo, 1980;
Kolb & Taylor, 1981; Ley & Bryden, 1979; Suberi & McKeever, 1977).
Although there may be concensus regarding the importance of the right
hemisphere in facial recognition, little is known about the relative roles of
different right hemisphere regions.
The major purpose of the current study was to compare the effects of cir-
cumscribed lesions of the frontal, parietal, and temporal cortex on the per-
ception of faces. For this purpose we chose a task devised by Wolff (1933),
the findings of which have been extensively replicated (Campbell, 1978;
Gilbert & Bakan, 1973; Lawson, 1978; Lindzey, Prince, & Wright, 1952;
McCurdy, 1949). In addition, at the suggestion of the late Professor H.-L
Teuber, we compared the perception of faces presented in both upright
and inverted positions in order to test the hypothesis that right posterior le-
sions handicap the recognition of faces presented in normal orientation but
do not affect the recognition of faces presented upside down (Yin, 1970).

METHOD
Subjects
In all, we studied 18 normal control subjects and 62 patients, each of the latter
having undergone a unilateral brain operation at the Montreal Neurological Hospital
for the relief of epilepsy. Table 1 gives the average age and Wechsler IQ ratings for
the patients subdivided according to locus of excision, together with the mean age
of the normal control subjects. All patients had speech represented in the left hemi-
sphere, as shown by pre-operative intracarotid sodium Amytal1 tests and/or neo-
cortical electrical stimulation of the cortex at the time of operation. Patient groups
will be described only briefly, since detailed accounts and diagrams showing the es-
timated extent of the lesions in these patients have been published (Kolb & Milner,
1981).

"Sodium amobarbitol — sodium Amytal, Eli Lilly and Co., Indianapolis, Ind., U.S.A.
 10 B. Kolb, B. Milner, & L Taylor

TABLE 1

Summary of Subjects Tested

Age Wechsler IQ
Subject Group N Mean Range Mean Range
Left frontal 6 27.1 21-44 103.5 80-123
Right frontal 8 26.3 15-48 100.2 79-123
Left parieto-occipital 9 28.7 12-39 101.4 79-117
Right parieto-occipital 6 23.3 17-28 97.4 70-123
Left temporal 16 26.7 15-44 109.9 84-129
Right temporal 17 27.7 16-48 111.5 85-146
Normal control 18 23.0 16-45 Not assessed

Frontal-lobe Groups: The lateral extent of removal in representative patients is il-

lustrated in Figure 1A. The removals from the right frontal lobe were typically some-
what larger than those from the left, since the latter spared Broca's area (as mapped
out by speech testing at operation). The frontal removals typically also included
parts of the anterior cingulate and subcallosal gyri on the medial aspect of the
hemisphere.
Temporal-lobe Groups: Figure 1B illustrates the lateral extent of temporal-lobe
removal for representative patients from the temporal-lobe groups. The mean extent
of cortical excision for patients with left temporal lobectomies was 5.0 cm (range
4.0-8.0) and for patients with right temporal lobectomies was 7.1 cm (range
6.0-9.5) along the base of the brain. The amygdala was partially or completely re-
moved in all cases. Among the patients with left temporal-lobe lesions, the hippo-
campus was spared in two cases and partially or completely removed in the remain-
ing cases. Similarly, among the patients with right temporal-lobe lesions, the hippo-
campus was spared in three cases and partially or completely removed in the re-
maining cases.
Parieto-occipital Groups: The parieto-occipital removals were quite heterogeneous
as to locus and extent, due in part to the need to respect the posterior speech zone
in the left hemisphere. The individual removals are illustrated in Figure 1C. Four exci-
sions on the left and one on the right totally removed the occipital lobe producing a
contralateral homonymous hemianopia. Two of the patients with left parietal-lobe le-
sions were tested in the early postoperative period and were dysphasic at that time.

Apparatus and Procedure

Following the procedure of Gilbert and Bakan (1973), 19 sets of stimulus pictures of
faces (9 male, 10 female) were produced in the same manner as the example in
Figure 2. Faces were photographed straight on, keeping the lighting as constant as
possible across the photograph. For 10 of the photographs, the comparison face
was in the normal orientation, and for the remaining 9, the comparison face was the
mirror-image of the normal orientation. This was intended to control for the possibili-
ty that the two halves of a face, as compared with the visual field they were in, were
differentially used as cues. Both comparison photographs were 14 by 18 cm in size.
The composite photographs were made of the two left and two right sides of the re-
spective comparison photographs, by cutting vertically through the middle of the
face. The opposite halves of the two photographs were mounted on black cardboard
 Perception of faces 11

A. FRONTAL B. TEMPORAL
Bo
Wa Do To. La. Ga. Se. B-

C. PARIETO-OCCIPITAL

An. St. Co. Be. Ph. Du. Ja. Fl

Ch. Ma. Hu. Fo.

El. Mu. Ce. Bz.

Ch. Al. Ro. Le.

Ch. Jo.

Figure 1. Diagrams based on the surgeon's drawings at the time of operation, showing the
estimated extent of cortical excision in representative frontal- and temporal-lobe and all
parieto-occipital-lobe cases.

to produce two symmetrical faces, as shown in Figure 2. The junction line was visi-
ble but seems to have been unobtrusive because no subject, when questioned later,
knew how the composite photographs had been constructed.
No precautions were taken to equalize lateral differences in hair style or facial ex-
pression, although no males with moustaches or beards were photographed, and all
persons were asked to assume a blank expression. The sex, the position of the left-
side or right-side composites below the unaltered comparison photograph, and the
type of unaltered photograph (normal versus mirror image) were all varied randomly
across the 19 sets of pictures.
Each set of three pictures was placed on a table directly in front of the subject,
who was then asked to choose which of the composite photographs most clearly
resembled the upper photograph. The subject was asked to give his impression of
12 B. Kolb, B. Milner, & L. Taylor

Figure 2. An example from the composite faces task. Above: normal photograph showing
facial asymmetry. Below: two symmetrical faces made by pairing, respectively, the left or
right half of the normal face with the corresponding mirror image. The subject must indicate
which of the composite photographs more closely resembles the real face.

overall similarity, to ignore the width of the faces, and not to let the relative attractive-
ness of the pair of composite faces influence the decision. After completing the 19
sets of photographs the subjects were kept occupied for approximately 45 minutes
with a variety of other tasks (Kolb & Milner, 1981; Kolb & Taylor, 1981) and then
retested; however, the stimulus booklet was inverted so that all of the photographs
were viewed upside down. Since the procedure using inverted faces was begun
somewhat later in the series, a small number of patients were not tested on it.
 Perception of faces 13

RESULTS

Upright Faces
Normal control subjects, patients with left-hemisphere lesions, and patients
with right frontal-lobe lesions all exhibited a mean preference of 65-70%
for the composite photograph matching the left side of the intact photograph
(right side of the comparison face), as can be seen in Figure 3A. In other
words, these subjects tended to choose the composite photograph corre-
sponding to that portion of the original photograph falling in their left visual
field. Patients with right temporal-lobe or right parieto-occipital lesions
failed to show a field bias, responding at chance levels to the two sides.
Simple analysis of variance showed a significant effect of lesion locus (F =
5.2, p < .01). Inter-group comparisons (Tukey's) revealed that the right
temporal and right parieto-occipital groups differed significantly from the
other groups (p's < .01).
The same results obtain when one looks at individual preference scores.
That is, 15 of the 16 patients with left temporal lesions, all 6 of the left fron-
tals, and all 9 of the left parieto-occipitals show a left field preference
(greater than 50%). In contrast, only 9 of the 17 patients with right temporal
lesions show a left field preference, as do 3 of the 6 right parietals and 5 of
the 8 right frontals. The size of the left field preference, when it is manifest-
ed, is also smaller in the right posterior lesion groups (range 31% to 68%)
than in the left lesion groups (47% to 84%), but is not smaller in the right
frontal group (38% to 84%).

Inverted Faces
When the faces were presented in the inverted position, the control subjects
again demonstrated a left visual-field bias as did the patients with left-
hemisphere lesions (Figure 3B). In contrast, patients with right-hemisphere
lesions showed chance selection of the composite photographs. Simple
analysis of variance yielded a significant effect of lesion locus (F = 2.6, p <
.05). Inter-group comparisons (Tukey's) showed the groups with right-
hemisphere lesions to differ significantly from the control group as well as
from the groups with left-hemisphere lesions (p's < .05).
Review of the individual data showed a pattern almost identical to those
for the upright faces, except that one patient with a left frontal lesion now
failed to show a left-field preference, and one additional patient with a right
frontal lesion showed no preference, making the number of right frontal pa-
tients who exhibited such preference 4 out of 8.

DISCUSSION
Our comparison of the effects of unilateral lesions of the frontal, temporal,
parietal, and occipital cortex upon the matching of photographs of human
14 B. Kolb, B. Milner, & L Taylor

A. UPRIGHT ORIENTATION

80 CONTROL LEFT HEMISPHERE RIGHT HEMISPHERE

7o^

60

50-
UJ
LL.
40
3 NORMAL FRONT. TEMP. PAR.-OCC. FRONT. TEMP. PAR.-OCC.
CO N 18 6 16 9 8 17 6

UJ B. INVERTED ORIENTATION

80 CONTROL LEFT HEMISPHERE

UJ
O
DC 7 n

60

50+H

40
NORMAL FRONT. TEMP. PAR.-OCC. FRONT. TEMP. PAR-OCC.
N 15 4 13 5 8 15 5

Figure 3. Histograms indicating mean percentage choice in favour of the left visual field for
upright (A) and inverted (B) orientation of the photographs in the composite faces task.

faces revealed a differential effect of these lesions upon the perception of

faces. In contrast to the left visual-field preference of control subjects and
patients with lesions of the right or left frontal, left temporal, or left parieto-
 Perception of faces 15

occipital cortex, patients with lesions of the right temporal- or right parieto-
occipital cortex displayed no visual field bias in their choice of composite
faces. These results are congruent with previous studies implicating the
right posterior cortex in face perception and face recognition (Benton &
Van Allen, 1968; Meadows, 1974; Milner, 1968, 1980; Newcombe, 1973;
de Renzi & Spinnler, 1966; Tzavaras, Hecaen, & Le Bras, 1970; Warrington
& James, 1967a; Yin, 1970), as well as with the more general claim that the
right hemisphere is dominant for visually-directed attention (Dimond, 1976;
Geschwind, 1977).
It is important to note that our results cannot be attributed to the pre-
sence of homonymous visual-field defects. The left-hemisphere groups
showed no exaggeration of the normal left-field bias, despite the fact that
the patients with left parieto-occipital lesions had right homonymous visual-
field defects that might have led them to favour the left side more than
normal subjects. Hence, the lack of left field bias in patients with right
posterior cortical lesions cannot be explained in terms of possible visual
field defects, nor even of a general diminution of perception in the opposite
visual field. It must also be pointed out that there was no evidence of con-
tralateral neglect in our patients with lesions of the right parietal cortex, as
judged by drawings or by bilateral simultaneous stimulation, thus ruling out
another possible explanation for the absence of a field bias.
The right frontal-lobe group showed a left visual-field bias for the percep-
tion of upright faces, but this preference declined significantly on the invert-
ed faces task. Further analysis of the responses of the patients with right
frontal-lobe lesions to the inverted photographs showed that four of the
eight patients perseverated on one response (left or right side of the page)
for most of the test, thereby scoring at a chance level. On the other hand,
the remaining four patients did not perseverate and exhibited the normal
left visual-field bias. Thus, although the group with right frontal-lobe lesions
failed to show a significant overall field bias, this result is confounded with
a perseverative response bias in several subjects. Perseverative behaviour
is common in patients with frontal-lobe lesions, particularly when perform-
ing difficult tasks (e.g., Milner, 1964). The perseverative behaviour in the in-
verted but not upright task by the patients with frontal-lobe lesions pre-
sumably occurred because of the more difficult perceptual analysis re-
quired in the inverted condition. Patients with right temporal or right parieto-
occipital lesions did not behave in this way, and they made an approximate-
ly equal number of responses to each side of the page.
The absence of a preferential choice for the left visual field in patients
with right temporal or right parieto-occipital lesions suggests that both of
these areas play a significant role in the normal left-field preference, and
thus in the normal processing of faces. The contribution of the temporal
region is supported by recent observations of visual cells in the temporal
lobe of the monkey that are selectively responsive to faces (Perret, Rolls, &
16 B. Kolb, B. Milner, & L. Taylor

Caan, 1979). Furthermore, right anterior temporal-lobe lesions have pre-

viously been shown to produce various changes in visual perception
(Kimura, 1963; Lansdell, 1968; Meier & French, 1965; Milner, 1958; Warr-
ington & James, 1967b). Similarly, the role suggested for the right posterior
cortex in facial processing is consistent with the poor performance of pa-
tients with right posterior cortical lesions on the Mooney Closure Test
(Milner, 1980), a task which eliminates normal contour lines in faces. It is
also consistent with the more general observation of impaired performance
on other complex visuo-perceptual tasks (Warrington & James, 1967b;
Warrington & Taylor, 1973).
The comparison between the upright and inverted presentations of the
composite photographs is relevant to the issue of whether or not there is an
orientation-specific face processor (Leehy et al., 1978; St. John, 1981; Yin,
1970). Yin (1970) drew attention to this possibility when he reported that
the memory of photographs of faces was impaired in patients with right
posterior lesions, but that this handicap was reduced when the photographs
were presented upside-down or when other complex visual stimuli, such as
houses, were presented instead. To date, there is little additional evidence
that bears on Yin's hypothesis regarding the "specialness" of faces, with the
exception of one or two tachistoscopic studies with normal subjects which
provide tentative support for his view (Leehy et al., 1978; St. John, 1981). If
the absence of a left visual-field bias for matching upright composite-faces
in the right posterior groups in the present study represents the interference
with an orientation-specific face processor, then one would predict from
Yin's (1970) experiment that there would be no difference between the
right posterior groups and the other groups on the inverted faces task. Our
data are, instead, consistent with the more parsimonious view that the
posterior part of the right hemisphere is specialized for the processing of
complex visual patterns, of which faces are a particularly striking example
(Ellis & Shepherd, 1975; de Renzi & Spinnler, 1966).

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