Differential right hemispheric memory storage of emotional and non-emotional faces

Neuropsychologia,

1977, Vol. 15, pp. 757 to 768. Pergamon Press. Printed in England.

DIFFERENTIAL RIGHT HEMISPHERIC MEMORY STORAGE OF EMOTIONAL AND NON-EMOTIONAL FACES* MAX SUBERI New Hampshire Hospital, Neuropsychiatric

Center, Concord, New Hampshire 03301, U.S.A.

and WALTER F. MCKEEVER Bowling Green State University, Bowling Green, Ohio 43403, U.S.A. (Received 24 Januavy 1977) Abstract-Seventy-two female subjects memorized two photographed faces and subsequently discriminated these “target” faces from two “non-target” faces. The faces were presented unilaterally for 150 msec, and manual reaction times for the discriminations served as the dependent variable. The face stimuli were either “neutral” or “emotional” in facial expression, these attributes having been shown, by a preliminary study, to be highly reliable. Faster reaction times were obtained for left visual field than for right visual presentation. Subjects (N = 36) who memorized emotional faces showed significantly faster discrimination of faces presented in the left than in the right visual field (25.7 msec); subjects (N = 36) who memorized faces lacking emotional expression also showed significant left visual field superiority (11.6 msec), but this left field superiority was significantly smaller than that of subjects memorizing emotional faces. Results are consistent with previous tachistoscopic evidence of right hemisphere superiority in face recognition speed and with diverse non-tachistoscopic evidence of preferential memory storage of affective material. The pattern of latencies for the different visual field-response hand conditions supported a model of lateral specialization in which the specialized hemisphere normally processes both directly-received and interhemispherically-transferred stimuli. INTRODUCTION CEREBRAL hemispheric specializations of function have come under intensive investigation in recent years. Evidence for the relative lateralization of language functions to the left hemisphere [l-3] and of visual-spatial functions to the right hemisphere [4-61 has accumulated steadily. A third function showing some degree of lateralization to the right hemisphere has been suggested by diverse observations. This function may be tentatively identified as “emotional memory” or “emotional imagery”, although its precise character remains to be clarified. The present experiment addressed the question of whether hemispheric differences could be found in the speed of recognition of emotional, as opposed to non-emotional, faces.

Tachistoscopic studies of face recognition latencies RIZZOLATTI, UMILTA, and BERLUCCHI [7] and GEFFEN, BRADSHAW and WALLACE [8] have *Based on a Doctoral Dissertation by the first al!thor. Supported by Grant Number NS-10414-04, from NINCDS, Public Health Service, to the second author. Reprints available from Dr. Walter F. McKeever, Department of Psychology, Bowling Green State University, Bowling Green, Ohio 43403, U.S.A. 757

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found left-visual field (right hemisphere) superiority in recognition speed for face stimuli; and PATTERSONand BRADSHAW [9] have found partial support for the hypothesis of faster left-visual field (LVF) than right-visual field (RVF) recognition of face-like drawings. These results are consistent with clinical evidence that inability to recognize faces or to interpret the meaning of facial expressions is usually associated with right-hemisphere damage [lo-131. It is generally assumed that the basis of the right hemisphere’s superiority for recognition of faces derives from its greater spatial ability. R~ZZOLATTI et al. [7] compared half-field reaction times (RT) for the recognition oi. photographs of male models. The models all projected a neutral, non-emotional expression, and in order to minimize isolated discriminative cues, they were clean-shaven and wore caps to cover their hair. The results showed a significant LVF superiority of 15.5 msec. The authors also reported a significant RVF superiority on RT to single-letter stimuli, demonstrating that the half-field superiorities depend on the spatial or verbal nature of the task. GEFFEN et al. [8] similarly found that manual RT for discrimination of target and nontarget faces was faster for the LVF. The LVF superiority averaged 25 msec. These investigators employed life-like Identi-Kit faces rather than actual photographs of people, and again the faces projected no particular emotional cues, although the faces were, in out opinion, all rather “unsavory” looking characters. Indeed, we would speculate that judgments regarding the affective projection of these faces would show them all to be projecting at least mildly negative affect. PATTERSONand BRADSHAW [9] employed schematic faces, each composed of stereotyped depictions of three features (eyes, nose, mouth). They found LVF superiority only when target and non-target faces differed on all three features, which they termed the “easy” discrimination. They found RVF superiority when the faces differed on only one feature, which they termed the “hard” discrimination. This latter finding appears contrary to what one would expect in view of demonstrations that the greater spatial ability of the right hemisphere is most evident under difficult discrimination conditions [14-161. The Patterson and Bradshaw study, however, may be questioned on several points. First, the stimuli bore little resemblance to real physiognomies; secondly, an analytic verbal set, rather than a global-spatial set, may have been more likely in the one-feature different condition; lastly, two of the matching faces in the “easy” discrimination were distinctly emotional (smiling and frowning mouths). In line with evidence of greater right than left hemisphere affective memory involvement, detailed below, it is possible that these affective cues contributed to the strong LVF superiority for that condition. In addition to the RT studies, several tachistoscopic studies employing simple recognition accuracy have also shown LVF superiority for face recognition [17-191. Thus, good evidence of LVF superiority for face recognition exists, but no study to date has examined the possible effects of facial-affect cues on recognition performance. Evidence of the relative lateralization of’ affective processes The earliest suggestions of differential hemispheric mediation of affective processes come from clinical observation. GOLDSTEIN [20] was the first to note a common emotional response to left-hemispheric lesions. He termed this response the “catastrophic reaction”. Subsequently, HBCAEN, AJURIAGUERRA and MASSONET [21] and DENNY-BROWN, MEYER and HORENSTEIN [22] described a complementary pattern of emotional response to righthemispheric lesions which they termed the “indifference reaction”. These patterns have been confirmed by GAINOTTI [23] in a study of 80 left-damaged and 80 right-damaged

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patients. The catastrophic reaction (anxiety, crying, hostility, compensatory boasting) was characteristic of left-cerebral damaged patients, while the indifference reaction (indifference, jocularity, minimization, anosognosia) was characteristic of right-damaged patients. These patterns have also been observed occasionally during sodium amytal deactivation of the left and right hemispheres [24]. There is also evidence of hemispheric asymmetry for affective memory processes. WECHSLER[25] found that short-term memory for the affective aspects of stories was more impaired by right- than by left-hemisphere lesions. Among normal subjects, too, dichotic listening evidence lends credence to the hypothesis that the right hemisphere is preferentially involved in short-term memory for affective stimuli. HAGGARD and PARKINSON [26], though not conceiving their study in terms of hemispheric specialization, found that judgments about the emotional tone (angry, bored, happy, distressed) of sentences heard in one headphone while “babble” was heard in the other, were significantly more accurate on left-ear presentations. CARMON and NACHSHON [27], who specifically set out to test the hypothesis of right hemispheric superiority for emotional dichotic stimuli, minimized verbal mediation in the task. Stimuli were tape recorded sounds of a child, a woman, and a man crying, laughing, and shrieking. Corresponding drawings of a child, a woman, and a man depicted as crying, laughing, or shrieking were made, and a preliminary study showed that the cross-modal correspondance was apparent to normal subjects. In the dichotic experiment proper, subjects listened to paired emotional sounds and on each trial indicated, by pointing with the right hand for right-ear stimuli and the left hand for left-ear stimuli, which of the nine pictures correspond to the sounds. Significantly greater accuracy in matching the auditory and visual forms of affective projection occurred when the sounds were heard in the left ear. Additional support for the greater role of the right hemisphere in emotional memory or imagery in normals comes from SCHWARTZ et al. [28] who recorded lateral eye movements (LEM) while subjects responded to questions having either emotional or neutral content. The verbal and spatial demands of the questions were also varied. When the results were collapsed across the verbal-spatial dimension, significantly more LEM to the left and fewer to the right were obtained for questions having emotional content. According to the rationale of LEM studies, this result indicated greater right hemisphere activation by emotional questions. Further research by this group [29] utilized recordings of parietal EEG patterns while subjects formed either visual or verbal images of past emotional experiences they had rated as intense. The visual images involved the subject picturing the actual events surrounding the experience while the verbal images involved him picturing himself describing the events in writing. No differences were found between the visual and verbal imagery modes, but significantly less alpha activity was recorded from the right hemisphere during the emotional than during the non-emotional periods. This suggested greater right- than left-hemisphere activation during emotional imagery. Additionally, females showed greater right hemisphere activation during emotional imagery than did males. The present experiment The present experiment addressed the possibility that differential magnitudes of LVF superiority (right hemisphere dominance) could be revealed in recognition latencies for emotionally expressive, as opposed to emotionally neutral, faces. The basic strategy involved varying the proportion of emotional and neutral faces and their target and nontarget status for different groups of subjects. The hypothesis was that the right hemisphere is more efficient in processing emotional stimuli than the left hemisphere. It was predicted

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that LVF superiority would obtain for neutral faces, as shown by others, but that the magnitude of LVF superiority could be augmented by making emotional cues either congruent or incongruent with the target and non-target categories. Thus, augmented LVF superiority was expected for the group exposed to either emotional target and neutral non-target faces or to neutral target and emotional non-target faces. In other words, the right hemisphere was expected to better appreciate emotional cues and to utilize them in discriminating target from non-target faces. Diminished LVF superiority was expected when both target and non-target faces all projected a specific affect, e.g. when all were either happy, sad, or angry faces. The identity of specific affect was expected to constitute a negative, or interfering, cue that would be largely overlooked by the left hemisphere but registered by the right hemisphere as a similarity which would blur the distinction between target and non-target faces. As will be seen, the predicted ordering of LVF superiorities did not obtain, but evidence nonetheless emerged that memory storage of emotional physiognomies is more lateralized to the right hemisphere than is memory storage of neutral faces. METHOD Subjects

Subjects were 72 right-handed female undergraduates at Bowling Green State University. experimentally naive and had normal or corrected-to-normal visual acuity.

All were

Stimuli

Stimuli were 16 photographs of the faces of four doctoral-level theater majors (two male, two female). Each model projected a “neutral”, “happy”, “sad”, and “angry” facial expression. The models were free of apparent facial hair, did not wear glasses, communicated the intended affects without opening their mouths, and wore hoods which covered their hairlines. The 16 photographs (Fig. 1) were chosen from a sample of 85 as being the least ambiguous in projecting the intended affects. A reliability study, with 20 undergraduate females, established the reliability of the intended affective expressions. Subjects were first asked to sort the pictures into two groups on the basis of the relative presence or absence of perceived emotional expression, and, after having done so, to sort of pictures they labeled “emotional” into three subgroups, each representing a qualitatively different emotion. Results showed four misclassifications on the neutral-emotional dimension (98.8 “/, agreement) and five on the specific affects among the emotional faces (97.97; agreement). Letters shown below the faces in Fig. 1 give the number and nature of misclassifications for each picture. The results demonstrated very high reliability, fully justifying the major independent variable manipulation of the tachistoscopic experiment. Following the reliability study, the stimuli were affixed to white posterboard cards suitable for tachistoscopic presentation. Photographs were 3.81 x 4.45 cm in width and height, corresponding to 2.0” and 2.3” of horizontal and vertical subtense, respectively, when viewed in the tachistoscope. The near- and far-points from fixation, therefore, equalled 0.5” and 2.8” respectively. In addition to the stimulus cards, 10 cards having only a single digit at the center were prepared. A solid black circle (0.5” diameter) served as the preexposure fixation target. Apparatus

Stimuli were presented in a Scientific Prototypes Tachistoscope (model GB) with luminances of the pre-exposure and stimulus fields set to 10 and 20 ft Im, respectively. Pilot data indicated that the task was quite difficult and dictated the luminances employed. Manual RT was obtained from a digital msec-reading Hunter Timer (model 22OC). The timer was started by the tachistoscopic exposure and stopped by the sub,jects’ manual button presses. All stimuli were exposed for 150 msec and viewing was binocular. Stimulus onset was triggered automatically by the termination of a 1.5 set warning tone. Three groups of 24 subjects were exposed to systematically varied stimulus conditions. GROUP NEUTRAL subjects were exposed exclusively to faces lacking emotional expression. Two of the stimulus faces (one male, one female) served as target and the other two served as non-target faces. The four neutral faces were counterbalanced such that each served equally often as target and non-target. As in all groups, subjects studied and committed to memory only the target stimuli prior to the discrimination task. GROUP EMOTIONAL subjects were exposed exclusively to emotional target and non-target faces. This group included three subgroups of eight subjects, each subgroup exposed only to happy, or sad, or angry faces. Stimuli were counterbalanced such that each of the 12 emotional faces served as target and non-target with equal frequency. The third group, designated GROUP MIXED, was exposed to both neutral and emotional faces.

Stimulus Person

*I

models

Person #2

Person

94

Intended offcct *Ne,utral” (N)

“Happy* (H)

*Sad*

“Angry” (A)

FIG. 1. Stimulus

faces used in the experiment.

I:p. 760

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Half of the subjects studied and committed to memory emotional faces and subsequently had to discriminate them from neutral non-target faces; the other half studied neutral faces and subsequently had to discriminate them from emotional non-target faces. Again, counterbalancing was applied so that the frequency of faces projecting a given affect and the sex of the models were equated across target and non-target stimuli. Procedure

After being introduced to the experimental setting, subjects were read instructions detailing the procedure. Following this, they were required to study, for a full 5-min period, the two target faces. At the expiration of the 5 min, the tachistoscopic trials commenced. A total of 160 discrimination trials (five blocks of 32) were conducted during a single session, the first block designated for practice and warm-up only. A total of 128 trials, 64 per field, therefore provided the data-base for analysis from each of the 72 subjects. Distributed within the blocks were 10 fixation-control trials. On these, a number from 2 to 9 appeared for 150 msec within the area of the fixation circle. Subjects were required to accurately report aloud what number appeared in the fixation circle at least PO% of the time. Those whose accuracy was less than PO% were excluded from the study (n = 3). Although there is evidence [30] that proper instructional set and random unilateral presentation are sufficient controls for visual fixation, the spot check was considered an added safeguard against subjects prone to deviate their fixation in accordance with guesses as to which field would contain the next stimulus. Subjects used either their right or left index finger for responses in each block of trials. The “same” and “different” buttons were arranged in a “forward” and “backward” configuration rather than a “left-right” configuration, and subjects began each trial with the index finger resting on a lucite square midway between the buttons.* The buttons (0.8 cm dia) were 2.4 cm apart. In order to ensure that onlv a discrete indexfinger response was possible, subjects were required to-keep the forearm resting on the-table and the heel of the hand on the response-button box. This eliminated any “thrusting” of the arm as a means of suppressing the buttons, an essential precaution against the possibility of ipsilaterally innervated proximal muscle response mediation. “Same” and “different” responses were counterbalanced across all hand-field conditions. Each block of trials contained 16 LVF and 16 RVF faces, half of them targets and half non-targets. A different random order of these features was employed within each block. Any trial in which a stimulus was incorrectly identified was repeated at the end of that block. Following each block, subjects were informed of their fastest and slowest RTs and encouraged to improve their performance by responding “as fast and as consistently fast as possible”. Subjects were never informed, of course, whether their fastest or slowest times had been on a LVF or RVF trial or on target or non-target faces. Three minutes for studying the duplicate photos of the target faces were provided at the end of each block. Without exception, subjects utilized the full 3 min for that purpose. Errors occurred on less than 5% of the trials and were unrelated to visual fields or to same-different judgments. Consequently, and as planned, RT served as the only dependent measure.

RESULTS Table 1 shows the median LVF, RVF and RVF minus LVF RT scores of all subjects, as well as the group mean RTs. It can be seen that LVF stimuli were discriminated faster than RVF stimuli in all groups. That the predicted ordering of LVF superiorities (GROUP MIXED, GROUP NEUTRAL, GROUP EMOTIONAL) was not obtained is apparent. The largest LVF superiority occurred for GROUP EMOTIONAL (mean superiority = 26.2 msec), the next largest for GROUP MIXED (18.1 msec) and the smallest for GROUP NEUTRAL (11.5 msec). A four-way ANOVA was applied to the data, the factors being GROUPS, FIELDS (LVF and RVF), response HAND (left and right), and RESPONSE (same or different). The analysis revealed only two significant effects. These were for FIELD (F = 28.0, df l/69, P < O.OOl), indicating LVF superiority across all other factors; and for RESPONSE (F = 21.6, df l/69, P < 0401), indicating faster responses to target faces (“same”) than to non-target faces (“different”). The overall LVF advantage over the RVF averaged 18.6 *Additionally, same-different responses were counterbalanced across forward and backward button presses between subjects. It was found that responses to the forward button were faster than to therear button, but this effect did not interact with any other factors.

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Table 1. Mean visual half-field reaction times, RVF minus LVF differences (DIF), and group means Group neutral RVF DIF

Group mixed LVF RVF

Group emotional LVF DIF RVF

Subject

LVF

1 2 3 4 5 6 7 8 9 10 11 12 I3 14 15 16 17 18 L9 20 21 22 23 24

564.8 756.8 664.5 766.8 709.5 620.8 696.5 671.3 754.3 695.0 598.3 567.8 816.3 729.3 741.8 704.5 686.3 773.8 694.8 771.3 594.0 780.8 557.8 712.5

575.0 789.8 677.3 873.3 714.8 644.0 683.0 699.8 755.0 665.3 665.3 570.3 846.3 725.5 746.5 696.3 661.3 819.3 692.8 759.0 612.3 795.5 578.8 660.5

10.2 33.0 12.8 106.5 5.3 23.2 -13.5 28.5 0.7 -29.7 67.0 2.5 30.0 -3.8 4.7 --8.2 -25.0 45.5 -2.0 -12.3 18.3 14.7 21.0 -52.0

554.0 617.3 615.0 592.5 725.5 655.5 665.5 724.5 710.3 685.8 750.5 771.3 4823 632.3 638.3 548.0 683.5 755.8 518.3 775.8 690.0 622.2 624.3 667.3

578.5 634.3 652.0 589.8 734.5 648.5 700.5 798.8 701.5 705.5 798.8 819.5 523.3 652.8 626.0 529.3 712.8 754.5 507.3 836.0 690.3 644.5 629.3 671.3

24.5 17.0 37.0 -2.7 9.0 -7.0 35.0 74.3 -8.8 19.7 48.3 48.2 41.0 20.5 ~-12.3 -18.7 29.3 --1.3 -11.0 60.2 0.3 20.3 5.0 4.0

721.0 756.5 825.0 627.5 657.3 760.5 669.3 800.5 631.3 549.8 622.0 645.8 846.5 644.5 618.8 726.5 629.0 627.8 627.8 715.0 726.0 778.0 627.0 579.3

700.8 829.8 832.5 650.8 677.5 773.5 725.5 839.0 679.3 575.0 657.0 674.5 915.3 689.8 650.0 736.3 583.3 666.0 623.3 721.3 690.8 842.0 652.5 656.8

- 20.2 73.3 7.5 23.3 20.2 13.0 56.2 38.5 48.0 25.2 35.0 28.7 68.8 45.3 31.2 9.8 -45.7 38.2 ___4.5

Group Means

692.9

704.4

11.6

654.4

672.5

18.1

683.9

710.1

26.2

DIF

6.3 ~~35.2 64.0 25.5 77.5

msec. The advantage of “same” over “different” judgments averaged 35.1 msec. Neither of these significant main effects interacted significantly with the other variables. The main effect of GROUPS was non-significant, although Table 1 indicates some trend for faster overall response in GROUP MIXED, where both spatial and affective cues could serve as bases for target-non-target discrimination. The main effect of HAND was also non-significant, and, indeed, left- and right-hand latencies were essentially identical (684.8 and 688.0 msec, respectively). Of course, the predicted interaction of GROUPS by FIELDS was non-significant. Planned tests of half-field differences within groups did reveal that the LVF superiority of GROUP NEUTRAL was somewhat short of statistical significance (P < O*lO), while the GROUP MIXED and GROUP EMOTIONAL LVF superiorities were significant (P < 0.01 and P
Left LVF

Right LVF

Left RVF

Right RVF

675.7

678.7

694.0

697.3

Table 2 gives the mean median RTs obtained for the various HAND-FIELD combinations across other factors. It can be seen that the ordering of RTs from shortest to longest was: (1) LVF-left hand; (2) LVF-right hand ; (3) RVF-left hand ; (4) RVF-right hand. It is also apparent that the LVF superiority magnitude was essentially the same, regardless of which hand made the motor response. i.e. there was no evidence of a FIELD

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by HAND interaction. Indeed, the mean RTs for homolateral (stimulus and response hand on the same side) and heterolateral responses (stimulus and response hand on different sides) differed by only 0.1 msec (686.4 and 686.3 msec). This suggests, as discussed later, that the right hemisphere was involved in processing both LVF and RVF stimuli. Finally, a planned test of possible LVF superiority differences for happy, sad, or angry faces within GROUP EMOTIONAL was conducted. Although interesting variations in LVF superiority occurred (sad = 36.5 msec; happy = 26.5 msec; angry = 15.8 msec), the small number of subjects in each specific affect condition and considerable variability precluded statistical significance of these differences. Upon completing the planned analysis and reviewing summary data, it appeared that a consistent and meaningful unanalyzed effect was evident in the data. Inspection of the performances of GROUP MIXED subjects showed that those who had memorized emotional target faces (the first 12 subjects of the group in Table 1) had a mean LVF superiority virtually identical to that of GROUP EMOTIONAL, while those who had memorized neutral target faces (the last 12 subjects in Table 1) had a mean LVF superiority similar to that of GROUP NEUTRAL. Thus, the LVF superiority of GROUP EMOTIONAL was 26.2 msec and that of the GROUP MIXED subjects who memorized emotional faces was 24.6 msec; the LVF superiority of GROUP NEUTRAL was 1 I.5 msec and that of GROUP MIXED subjects who memorized neutral faces was 11.6 msec. This suggested that the critical determinant of half-field differences magnitudes was whether subjects had memorized emotional or neutral faces, regardless of the nature of the non-target faces. It was noteworthy in this connection that, almost without exception, subjects expressed surprise that the non-target faces looked “like that” when they were allowed to examine them after the experiment. Apparently, faces seen only in the tachistoscope were minimally appreciated beyond the fact that they were not the faces memorized. To evaluate this hypothesis, the subjects were regrouped into those who had memorized emotional faces (n = 36) and those who had memorized neutral faces (n = 36). It should be clear that these two groups were constituted on the basis of their identical memory task assignments. A four-way ANOVA, with the same factors as in the previous analysis, was applied to the regrouped data. Three significant effects were obtained. Two of these, for FIELD and for RESPONSE, were, of course, identical to the previous analysis. The third, and critical one for the memory effect hypothesis, was the interaction of GROUPS by FIELDS (F = 4.13, df = l/70, P < 0.05). Thus subjects who had memorized emotional faces did exhibit significantly greater LVF superiority (mean = 25.7 msec) than those who memorized neutral faces (mean = 11.6 msec). Two one-way ANOVAs were computed to test the significance of LVF superiority within the two groups. For those memorizing emotional faces, the LVF latencies were significantly shorter than those of the RVF (P < 0.001); for those memorizing neutral faces the LVF latencies were also faster than those of the RVF (P < 0.05). Thus, evidence of right-hemispheric superiority obtained for both groups but with a significant enhancement of that superiority for those memorizing emotional faces. DISCUSSION It was originally proposed that the correspondance of emotional and neutral facial expressions to target and non-target categories of stimuli would enhance LVF superiority and that the presence of a specific affect common to all stimuli would diminish LVF superior-

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ity. These predictions were deduced from the hypothesis that the right hemisphere was perceptually more sensitive to affect cues and that affect cues irrelevant to target-non-target discrimination would constitute a similarity adversely affecting discrimination performance of the right hemisphere. The hypothesis was not supported. However, the debriefing procedure following the experiment revealed that subjects had generally been unable to appreciate the stimulus characteristics of non-target faces. Had subjects studied both target and non-target faces, or had the viewing conditions been made easier in some manner, it is possible that the predictions would have been borne out. Despite the failure of our original predictions, evidence of a greater preferential storage of emotional than neutral faces to the right hemisphere emerged. Subjects who memorized emotional faces showed a significantly greater LVF superiority than subjects who memorized neutral faces. Since LVF superiority also obtained for the neutral target faces, the results indicate that the presence of emotional expression in face stimuli augments the right hemisphere’s superiority over the left. This is also indicated by the fact that the differences between hemispheres in discrimination time were virtually all due to increased left-hemisphere latencies for emotional over neutral-face stimuli. Thus, whatever the mediating mechanism of greater right hemisphere superiority for the memorization of emotional faces may be, it is not additive with that mediating memorization of neutral faces. Consequently, the results are not compatible with their possible explanation in terms of spatial ability differences. Such an explanation would suggest that emotional faces may be simply more complex in spatial terms than neutral faces, and that there is no need to posit differential laterality for “emotional memory” when just plain “spatial memory” will suffice. The consistent absence of any suggestion of a significant GROUPS effect runs counter to the argument that emotional faces are spatially more difficult than neutral faces. The latencies do not reflect any increased difficulty. Although there is a need for further study of the relationship of visuo-spatial processes to affective memory-storage processes, we are inclined to the view that they are not necessarily positively correlated. Indeed, the bulk of evidence suggests that females are only weakly right hemisphere specialized for spatial processing and strongly right hemisphere specialized for affective memory storage, while the converse pattern obtains among males. Present findings indicate that the presence of affective expression in faces produces greater right hemisphere pre-emption of the memory-storage process. This is consistent with WECHSLER’S[25] finding that the right hemisphere assumed the major role for storage of the affective quality of narrative text, with studies employing emotional reflective questions and instructions to visualize emotional experiences [28, 291, and with dichotic listening findings [26, 271. It is, to the best of our knowledge, the only evidence of such a hemispheric difference observed via the lateralized tachistoscopic methodology, and, as such, it is an additional demonstration of the power of this methodology for the study of hemispheric asymmetries of function. That the nature of stimuli memorized proved to be the determinant of differential LVF superiorities suggests that the relative lateralization of memory processes for particular stimulus classes may be basic to “perceptual asymmetries”. Indeed, “recognition” can occur only for stimuli stored in memory. A recent study by MOSCOVITCH, SCULLION and CHRISTIE [31] of latencies for discrimination of face stimuli has demonstrated that when pure devoid of memory or other higher level cognitive demands, is “perceptual discrimination”, required, no hemispheric differences obtained. When subjects had to discriminate memorized

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FACES

765

from non-memorized faces, however, these investigators found significant right hemispheric superiority. The findings also provide essential replication of previous demonstrations of LVF superiority for discriminating target from non-target faces. The condition most similar to that of RIZZOLATTI et al. [7], the GROUP NEUTRAL condition, yielded a slightly smaller LVF superiority magnitude than obtained by Rizzolatti et al. and a substantially smaller proportion of LVF superior subjects. Ninety-two per cent of their subjects showed faster LVF than RVF latencies, whereas only 67% of our GROUP NEUTRAL and GROUP NEUTRAL plus GROUP MIXED subjects exposed to neutral targets showed faster LVF times. This might well reflect the fact that all the subjects of Rizzolatti et al. were males, while ours were females. If discrimination between target and non-target neutral faces is mediated by spatial cues alone, one might expect the males, who are thought to be more right hemisphere dominant for spatial ability (see [32, 33]), to show greater LVF superiority for neutral-face stimuli. Females were chosen for the present experiment on the basis of DAVIDSON and SCHWARTZ’S [29] finding of greater right hemisphere activation among females when recalling emotional experiences. Now that an effect of emotional cues on half-field recognition latencies for face discrimination has been shown, it would be interesting to see if males show comparable neutral-emotional stimuli effects. The results also provide further information regarding a question bearing on the validity of differing models of cerebral dominance. In tasks such as simple light-onset detection, a response hand by visual field interaction typically obtains, with faster RTs associated with homolateral stimulus-response combinations [34-361. In such a task, both hemispheres process (detect) the stimulus material equally well, and no main effect of visual field of stimulus presentation is found. This may be termed a “no dominance” model, with RTs varying only as a function of lengthened latencies consequent to the need for interhemispheric communication between the hemisphere receiving the stimulus and that initiating the manual response. The analysis of HAND-FIELD interactions to assess the degree of cerebral dominance for tasks showing significant dominance (field) effects is also possible. If each hemisphere can process the stimulus material, but one hemisphere excels the other (a “relative” cerebral dominance model), one would expect a significant FIELD by HAND interaction and a particular ordering of latencies. For a task processed better by the right hemisphere, that ordering, from fastest to slowest, for the various hand-field combinations would be: (1) LVF-left hand; (2) LVF-right hand; (3) RVF-right hand; (4) RVF-left hand. This, of course, makes the reasonable assumption that stimulus processing time requirements are greater than transcallosal transfer time. If both hemispheres can process the stimuli, but with different efficiencies, the above ordering would obtain because only combinations 2 and 4 (heterolateral conditions) would require an interhemispheric transfer from a processing to a response-initiating hemisphere. Neither combinations 1 or 3 (homolateral conditions) would require such a time-consuming transfer. No interaction of hand and visual field was obtained in the present experiment, and homolateral responses, predicted to be faster than heterolateral responses by this model, were identical to the heterolateral responses in mean latency. The alternative model, that the superior hemisphere is involved in all the processing, predicts no FIELD by HAND interaction, fastest discrimination of face stimuli in the LVF-left hand condition, and slowest discrimination in the RVF-right hand condition. The LVF stimuli project to the right hemisphere, and in the left hand response condition, require no interhemispheric transfer for response initiation. In the RVF-right hand con-

766

MAX SKJBERI and WALTER F. MCKEEVER

dition, the stimuli would have to be transferred to the right hemisphere for processing (target-non-target correspondence) and a second transfer back to the left hemisphere for initiation of the motor response would be required. The LVF-right hand and RVF-left hand conditions would each require one interhemispheric transfer, but the nature of that transfer would differ. In the LVF-right hand condition, a simple, post-decisional transmission would occur, while in the RVF-left hand condition the transmission would involve a more complex “raw” visual pattern for discriminative processing. Thus, the predicted ordering of this model (LVF-left hand; LVF-right hand; RVF-left hand; RVF-right hand) was actually obtained. This supports the notion that in normal subjects, the inferior hemisphere for processing a given class of material either relinquishes that processing or is inhibited from the processing by the superior hemisphere. The findings are consistent with Moscovrrc~~‘s [37] theorizing that the apparently greater capacity of each hemisphere for its “inferior” function, suggested in split-brain studies, occurs only by virtue of the disinhibiting effects of commissorotomy. Finally, the consistently faster RTs for “same” than for “different” judgments obtained can best be understood as the inevitable result of the greater familiarity of target than of non-target stimuli. No evidence for an interaction of this effect with any other factor was obtained. REFERENCES laterality in left-handed aphasics. Brain 77, 521-548, 1954. 1. GOODGLASS, H. and QUADFASEL, F. Language University Press, Princeton, 2. PENFIELD, W. and ROBERTS, L. Speech and Bruin Mechaniswzs. Princeton 1959. sodium amytal for the lateralization of cerebral 3. BRANCH, C., MILE;ER, B. and RASMUSSEN, T. lntercarotid speech dominance. J. Neurosurg. 21, 399405, 1964. 4. WARFUNGTON, E. K. and KINSBOURNE, M. Drawing disability in relation to laterality of lesion. Brain 89, 53-82, 1966. maze learning in man: effects of unilateral cortical excisions and bilateral 5. CORKIN, S. Tactually-guided hippocampal lesions. Neuropsychologia 3, 339-351, 1965. of bilateral chimeric figures following hemi6. LEVY, J., TREVARTHEN, C. and SPERRY, R. W. Perception spheric deconnection. Brain 95, 61-78, 1972. superiorities of the right and left cerebral 7. RIZZOLATTI G., UMILTA, C. and BERLUCCHI, G. Opposite hemispheres in discriminative reaction time to physiognomical and alphabetical material. Brain 94, 431442, 1971. effects on reaction time to verbal and 8. GEFFEN, G., BRADSHAW, J. L. and WALLACE, G. Interhemispheric nonverbal stimuli. J. exp. Psychol. 87,415422, 1971. hemispheric mediation of nonverbal visual slimuli. 9. PATTERSON, K. and BRADSHAW, J. L. Differential J. exp. Psychol.: Human Percept. and Perform. 1, 246-252, 1975. .4.1M.A. Archs Neural. 7, 92-100, 10. HI?CAEN, H. and ANGELERGUES, R. Agnosia for faces (prosopagnosia). 1962. in brain damaged patients. Nerr/,o/ogy 16, 145-152, 11. DERENZI, E. and SPINNLER, H. Facial recognition 1966. and recall after right temporal lobe excision in man. Newopsychologiu 6, 12. MILNER, B. Visual recognition 191-209, 1968. by brain injured patients. A dissociable ability? Neuropsycholo,qin 8, 13. YIN, R. K. Face recognition 395-402, 1970. in the recognition of verbal and nonverbal stimuli in man. 14. FONTENOT, D. J. Visual field differences J. camp. physiol. Psychol. 85, 564-569, 1973. and lateral differences in perception and memory. 15. DEE, H. L. and FONTENOT, D. J. Cerebral dominance Neuropsychologia 11, 167-173, 1973. recognition of Japanese letter materials in the left and right 16. HIRATA, K. and OSAKA, R. Tachistoscopic visual fields. Psychologia 10, 7-18, 1967. laterality effects on a facial recognition task in normal subjects. Cortex 9, 17. H!LLIARD, R. D. Hemispheric 246-258, 1973. for recognition of words and faces in good and poor 18. MARCEL, T. and RAJAN, P. Lateral specialization readers. Neuropsychologiu 13, 489-497, 1975.

DIFFERENTIALRIGHT HEMISPHERICMEMORY

STORAGEOF EMOTIONALAND NON-EMOTIONAL FACES

167

19. KLEIN, D., MOSCOVITCH, M. and VIGNA, C. Attentional mechanisms and perceptual asymmetries in tachistoscopic recognition of words and faces. Neuropsychologia 14,55-66,1916. 20. GOLDSTEIN, K. The Organism: A Holistic Approach to Biology, Derivedfrom Pathological Data in Man. American Books, New York, 1939. 21. HBCAEN, H., AJURIAGUERRA, J. and MASSONET, J. Les troubles visuo-constructifs par lesion parietooccipitale droite. Role des perturbations vestibulaires. Enckphale 1, 122-179, 1951. 22. DENNY-BROWN, D., MEYER, J. S. and HORENSTEIN, S. The significance of perceptual rivalry resulting from parietal lesions. Brain 75, 433-471, 1952. 23. GAINOTTI, G. Emotional behavior and hemispheric side of the lesion. Cortex 8,41-55,1972. 24. PERRIA, L., ROSADINA, G. and ROSSI, G. F. Determination of side of cerebral dominance with amobarbital. Archs Neurol. 4, 173-181, 1961. 25. WECHSLER, A. F. The effect of organic brain disease on recall of emotionally charged vs neutral narrative texts. Neurology 23, 130-135, 1973. 26. HAGGARD, M. P. and PARKINSON, A. M. Stimulus and task factors as determinants of ear advantages. Q. JI exp. Psychol. 23,168-177, 1971. 27. CARMON, A. and NACHSHON, I. Ear asymmetry in perception of emotional non-verbal stimuli. Acta psychol. 37, 351-357, 1913. 28. SCHWARTZ, G. E., DAVIDSON, R. J. and MAER, F. Right hemisphere lateralization for emotion in the human brain: interactions with cognition. Science 190, 286288, 1975. 29. DAVIDSON, R. J. and SCHWARTZ, G. E. Patterns of cerebral lateralization during cardiac biofeedback vs the self-regulation of emotion: sex differences. Psychophysiology 13, 62-74, 1976. 30. MCKEEVER, W. F., SUBERI, M. and VANDEVENTER, A. D. Fixation control in tachistoscopic studies of laterality effects: comment and data relevant to Hines’ experiment. Cortex 8,473%478, 1972. 31. MOSCOVITCH, M., SCULLION, D. and CHRISTIE, D. Early vs late stages of processing and their relation to functional hemispheric asymmetries in face recognition. J. exp. Psychol.: Human Percept. and Perform. 2,401406, 1976. 32. KIMURA, D. Spatial localization in the left and right visual field. Can. J. Psychol. 23,445-458, 1969. 33. MCGLONE, J. and DAVIDSON, W. The relation between cerebral speech laterality and spatial ability with special reference to sex and hand preference. Neuropsychologia 11, 105-113, 1976. 34. JEEVES, M. A. A comparison of interhemispheric transmission times in acollosals and normals. Psychon. Sci. 16, 245-246, 1969. 35. BRADSHAW, J. L. and PERRIMENT, A. D. Laterality effects and choice reaction time in a unimanual twofinger task. Percept. Psychophys. 7, 185-187, 1970. 36. BERLUCCHI, G., HERON, W., HYMAN, R., RIZZOLATTI, G. and UhnL%, C. Simple reaction times of ipsilateral and contralateral hand to lateralized visual stimuli. Brain 94,419-430, 1971. 37. MOSCOVITCH, M. On the representation of language in the right hemisphere of right-handed people. Brain and Language 3,47-71, 1976.

72 fenmes ges et ensuite visages ment

avaient

devaient

Les

I'non cibles".

pendant

mination

150 msec.

Staient

soit

(dans USE Etude

plus

rapide

dans

le champ

visages

pour

6tait

tation

dans

superiorit&

les sujets cette

Ces rPsultats

sujets

gauche

qui m6morisaient

sont en accord sur la supEriorit

l'expression avaient

BLE

temps de rGact1on

le champ

visuel

des visages

plus rapide

Stalt

de discri-

Les stimulus

gauche

que

(n = 36) qui memorisaient

(25,7 msec.). du champ

manuelle

selon

des

visuel

(n = 36) qui rknorisaient

sup@rioritS

des

dans

les sujets

droit

signlficative

chez

anterleures

Chez

significativement

nais

A celle

On a obtenu

de 2

unilaterale-

cfs attributs

la discrimination

le champ

pr6sentSs

"¬ionnels"

la prgsentation

¬ionnels,

gauche

soit

de visa-

"cibles"

dependante.

prGliminaire,

flables).

droit.

dtaient

la variable

"ncutres",

trouvf?s hautement

visages

ces visages

et les temps de r&action

representalent

faciale

2 photographies

B m&noriser

discriminer

pr&sentSs

des d

que lors de la pr&sen-

On constatalt gauche

des visages

significativement des visages

avec des Gpreuves de 1'hPmisphSre

aussi

une

(11.6 msec.) uncutres", lnfcrieure

"6motlonnels". tachistoscopiques droit

dans

la vi-

MAX SUBERI and WALTER F. MCKEEVER

768

Deutschspractiige Zusammenfassung: 72 wcjhliche

'Tersuchspersonen sollten sich zwei photographi-

sche Cesichter

merken und anscblieOend

von zwei andercn Gesichtern

diese "Ziel"-Gesichter

unterscheiden.

Die Gesichter

den im halben Gesichtsfeld

15 msec leng dargeboten;

fiir die manucll vcllzogenc

Rcaktion

Variable

fiir die Diskrimination.

Gesichter

waren entweder

vorausgegangenen hoch reliabel

Untersuchung

gezeigt,

(N = 36),

diskriminierten

wenn die Gesichter msec).

in signifilcant kiirzeren Zeiten,

in linken Gesichtsfeld

Die Versuchspersonen

nifikante

als fur die in rechten. Die

die die "emotionalei;" Gesichter

Komponente

pr3sentiert

wurden,

im rechtei? Gesichtsfeld

(25,7

(N = 3'>), die die Gcsichter

ohne

mit einer Darbietung

emotionale

einer

clan diese Attribute

sind. Fiir die Llarbiztung im linken Gesichtsfeld

Versuchspersonen

verglichen

in Bezug

denn es hatte sich anl5Olich

genlligtenkiirzere Reaktionszeiten erinnerten,

client2 31.5 abhsngige

Die als Sl;imuli verwandten

"neutral" oder "emotional"

auf den Gesichtsausdruck,

wur-

die Zeit

erinnerten,

zeigte!: ebenfalls

eine sig-

Linksfeliiiihcrlega?~hr?it ('II,6 msec), a?>er diese

Linksfeldiiberlegenheit

war signifikant

don Vcrsnchspr~rsonc~i, die die Gesichter Romponente

erinnerten.

Die Ergebnisse

frii:lerentacbistoskopischen schc!! Uberlegerheit

gerinTer ~, als die bci mi-t der 2:j.c tionalcn

stimmen iiberein illit

Befunde;] zur l~ech.ts!?emispii'iri-

bci.m ~esiclltseriterlilcll unil mit verschiede-

nay, nicht-tacki s tos!
Material

in der rechten Hezaisphare. Die Lstenz-

fiir die verschiedenen

feldreizung

und nanuell bewirkter

Nodell einer halbseitigen lisierte

Gegcbenheiten Reiz-Antwort

Spezialisierung,

I!emisph;irenormalerweise

siiitzen tlas

in der die spezia-

sowohl die dirck-t erhalte-

nen, wie such die interhemisphgrisch aufarbeitet.

von Gcsichts-

weitergelciteten

Stimuli