Neuropsvcholoqzo. Vol. 28. No. 2. pp. 199-209. 1990 Prmled m Great Bntam

c

0028-3932’90 S3.00+0.00 1990 Pcrgamon Press plc

LATERALIZATION FOR THE EXPRESSION AND PERCEPTION OF FACIAL EMOTION AS A FUNCTION OF AGE CARIDAD R. MORENO,*? JOAN C. BOROD,$ JOAN WELKOWITZ§ and MURRAY ALPERT* tDepartment of Psychology, Northside Center for Child Development, New York, U.S.A.; ZDepartments of Psychology, Queens College, and Neurology, Mount Sinai Medical Center, The City University of New York, U.S.A.; SDepartment of Psychology, New York University, U.S.A.; and CDepartment of Psychiatry. New York University Medical Center, U.S.A. (Received 3 Nooember

1988; nccepted 23 Julp 1989)

Abstract-In order to test the hypothesis of right hemisphere changes with age. this study examined lateralization for facial emotion in young, middle-aged, and older women (N=90). For expression, subjects were photographed while posing positive and negative emotions. Composite photographs were created and rated for intensity. For perception, subjects were required to make intensity judgements about emotional chimeric faces. Overall. subjects demonstrated significant left-sided facial asymmetry for expression and significant left hemispace biases for perception. The findings for facial expression were not influenced by emotional valence or resting face asymmetries. There were no changes in lateralization as a function of age for either expression or perception. Taken together. these findings lend support to the notion that the right hemisphere mediates emotional processing across the adult life span.

INTRODUCTION THE LITERATUREregarding hemispheric changes with age suggests that there is a decline in functions mediated by the right hemisphere, while those of the left hemisphere remain relatively stable throughout the life span [ 1. 11,281. BROWN and JAFFE [ 1 l] have proposed a theory of brain development suggesting that lateralization is a continuous process which extends throughout the life span. The studies testing this “aging hypothesis” have examined language (e.g. [ 17, 27, 38]), visuospatial processing (for review, see Cl]), somatosensory functions [24, 411, and motor abilities [21, 401. While some of these studies utilized performance measures, typically procedures have been used which provide for lateralized input of stimulus materials (e.g. via dichotic listening) to the left or right side of the body (e.g. ear). Superior performance with input to a given side is interpreted as reflecting greater involvement of the contralateral hemisphere. Although the bulk of the literature suggests a decline in right hemisphere functioning with age, contradictory studies with no age-related changes in lateralization have also been reported (e.g. [S, 391). To date, the studies examining the right hemisphere and aging hypothesis have focused on cognitive and motoric functions. Virtually no attention has been directed to affective functions, which also are assumed to be mediated by the right cerebral hemisphere. It is

*Address for correspondence: Dr Caridad New York City, NY 10029, U.S.A.

Moreno.

Northside

199

Center for Child Development.

1301 Fifth Avenue.

200

CARIDAU R. MORENO, JOAS C. BOROU. JOANWELKOWITZ and

MURRAY ALPERT

important to note that there is evidence for affective and emotional changes with age. Research has shown that with increasing age individuals tend to become more introverted, more cautious, and less emotionally responsive to the external environment [lo. 37. 423. Recently, MALATESTA and IZARD [34] have suggested that emotional expression may be attenuated in the elderly. Finally, affective disturbances and depression have been commonl> noted in the elderly [3]. The current study was designed to extend the examination of changes in right hemisphere functions with age from the cognitive to the affective domain. Measures of emotional expression and perception were administered to groups of young, middle-aged. and older normal adults. These measures were employed since there is substantial evidence that the right hemispere is involved in emotional processing [S, 14,45,47]. The face was chosen as the specific communication channel since it provides lateralized indices in normal subjects for hotlz expression and perception of emotion. To measure lateralized changes in expression, facial asymmetry during posed emotional expression was examined. using paradigms developed by B~RCID et al. [4,9]. To measure lateralized changes in perception, hemispace biases for judgements of emotional chimeric faces were studied, using the paradigm developed by LEVYet al. [32]. If right hemisphere functions are compromised with age, one would expect decreases in the magnitude of the typical left-sided biases on these tasks as one moves from the youngest to the oldest subject group.

METHODS Suh/rct.s Subjects were 90 right-handed females who were selected accordmg to age: young group = 21 39 years. mtddle-aged group = 4tX 59 years. and older group = 60-8 1 years. There were 30 subjects in each group. Female subjects were studled since there is evidence to suggest that females are more lateralized [7.46] and more expressive [I-?] than males on tasks of emotional processing. Subjects were ri_eht-handed by self-report. writing hand. and handedness inventory [IX]. Subjects who were originally left-handed but were trained to wrote wtth their right hand were excluded from the study. All subjects were evaluated for lateral preference [18]. since a relationship between facial asymmetry and lateral dominance has been found by some m\‘estigators (e.g. foreyedness [4.3?]). Overall. subjects were strongly right-handed. strongly right-footed. and right-eyed. Familial left-handedness was determined accordmg to the presence or absence of left-handedness in at least one parent or a full sibling. See Table 1 for group means for laterality and demographic variables. When analyses of variance were conducted to examine group differences on the laterality variables. there were no significant main effects of age group. All subjects were wjhite. were native or fluent speakers of English. and had at least a ninth-grade education (see Table I ). Although there was a significant main effect of age group for years of educatton (F= 5.98: d.f. =2.87; /‘ are graphIcally displayed for each age group in Fig. 2. In addition. a lateralit) ratio ([left hemiface right hemiface] [left hemiface +right hemifdce]) was calculated from the intensity ratmgs for each expresbton.

Procrdure.\. To examine laterdlized perceptlon. a free-field vision task developed b> L~~\Y LV111.[32] was used. This task consists of 36 pairs of non-congruent chimeric faces. in which one half of a poser’s face IS smiling u hlle the other half displays a neutral expression from the same poser. Two chimeric faces. the origmal and Its mirror-image. are mounted one above the other on an Xf x 11 in. sheet of paper. Subjects are asked to looh at each pair and to report which chlmerlc face appears happier (“top”. “bottom“, or “both the same”). Scr~-~nq. In scormg performance on the chimeric faces task, “left” represented the number of”happler” judgements m which the chimerlc face wtth the smile in the subject’s left hemispace was perceived as happier. and vice versa for “rlght”. The number of left responses and the number of right responses were determmed for each subject. These data are dlsplayed for each age group in Fig. 3. In addition, using the LEVY er al. procedure [31]. a laterality ratio ([left hemlspace right hemispace]:36) was calculated for each SubJect. The denominator. 36. represents the number of pairs of chimerlc faces in the task.

RESULTS Anulyses

cf t;uriance

on the facial

asymmetry

dutu

To test the hypothesis of changes in facial asymmetry as a function of age, an analysis of variance (ANOVA) was conducted on the data for Age Group (young, middle-aged, older), Hemiface (left, right), and Emotion (happiness, pleasant surprise, sadness, disgust). A 3-way repeated-measures ANOVA (3 x 2 x 4) was conducted on the mean intensity ratings. There was no significant interaction between Age Group and Hemiface (P > 0.900) or among Age Group, Hemiface, and Emotion (P>OSOO). There was, however. a significant main effect for Hemiface (F= 11.11; d.f. = 1,87; PO.500) suggests that patterns of hemiface intensity were consistent across emotional expressions. In addition, there was a significant main effect of Emotion (F=88.68; d.f.=3,261; P O.800). there was a significant interaction between Age Group and Emotion (F=2.67: d.f. =6. 261; P-cO.05). When age group differences were examined for each emotion. post hoc tests revealed significant differences only for disgust. which was expressed more intensely by the older than by the young or middle-aged group. When emotion differences were examined for each age group. each of the other emotions was more intense than sadness for all groups. For the young group, surprise was more intense than disgust and happiness. For the older group, surprise was more intense than happiness. and disgust was more intense than both happiness and xurprisc. To examine the effect of emotional valence on hemiface intesity, emotions were grouped into their respective valence categories and a mean intensity score calculated for the two positive and the two negative emotions. A 3-way repeated-measures ANOVA (3 x 2 x 2) was conducted on the intensity scores for Age Group. Hcmiface. and Valence. Again. there was a main cffcct of Hemifacc (F= 1 1.I 1: d.f. = I. X7: P_(O.OOl ) but no interaction between Valence :md Hcmiface (P> 0.200) or among Age Group. Valcncc. and Hemifacc (P >0.600). While there \vas ;I main ctlkt for Valence (F= 27.76: d.f. = 1. 87: P 0.800) Age Group by Valence (P > 0.05) or Age Group by Hemiface (P~O.900). Analyses

qf cariance

on the lateralitj~

ratios

The laterality ratios were used to examine lateralization across the age groups because. although this index does not permit the evaluation of individual hemiface or hemispace effects, it does provide a correction for differences in base performance. To examine changes in facial asymmetry, a 2-way ANOVA (3 x 4) was conducted on the laterality ratios for Age Group and Emotion. None of the findings for Age Group (P> 0.800). Emotion (P>O.SOO), or Age Group by Emotion (P>O.400) was significant. To examine changes in perceptual bias. a l-way ANOVA (3) was conducted on the perception laterality ratios for Age Group. There was no significant effect of Age Group (P>O.O5). Finally, the laterality ratios were examined to determine whether they were significantly left-sided. using a t-test against a mean of 0 (symmetry). The overall laterality ratios for expression (_Y= +0.014; t=3.18, d.f.=89. P~0.01) and perception (X= +0.327; r=6.87. d.f.=89. P < 0.001) were significantly left-sided.

CARIDAD R. MORENO, JOAN C. BOROD, JOAN WELKOWITZ and MURRAY ALPERT

206

Distribution

qf laterality

ratios

To examine further the hypothesis of changes in facial laterality as a function of age, expression and perception laterality ratios for individual subjects were inspected. For expression, a mean ratio score was computed across the four emotions, since there were no significant effects for Emotion in the ANOVA reported above. Frequency distributions were constructed for both data sets regarding the number of subjects with left-sided laterality ratios (greater than zero), right-sided laterality ratios (less than zero), and left-sided equal to right-sided laterality ratios (equal to zero) (Table 2). As can be seen in Table 2, subjects were more left-sided when expressing and perceiving facial emotion. Chi-square tests were conducted to examine distrubutions of laterality ratios by comparing the number of subjects obtaining left-sided ratios vs the number of subjects obtaining right-sided or equal ratios. There were no significant differences as a function of age for the expression (P> 0.800) or the perception (P~0.10) task. Table 2. Frequency

distributions

for expression and perception by age group

Direction of laterality ratio

Task

Young

laterality

Age group Middle-aged

ratios.

separately

Elderly

Expression*

Left-sided Equal: Right-sided

2ot 0 10

I8 0 12

20 0 10

Perception

Left-sided Equal Right-sided

25 3 2

18 0 12

22 0 8

*Laterality ratio represents the mean of the four emotions. tAll entries are the number of individual subjects. ZLaterality ratios of zero were assigned to the equal category

Correlational

analyses

Finally, to address the aging hypothesis using the full range of scores, laterality ratios for each task were correlated with age (in years) for all subjects. As would be expected from the results above, coefficients were not significant for expression (r= -0.08) or for perception (r= -0.15).

DISCUSSION The primary hypothesis examined in this study was that subjects would exhibit decreases in facial asymmetry and perceptual bias with age. This hypothesis was not supported by any of the statistical analyses. For perception, our findings are consistent with two other studies using facial stimuli. OBLER et al. [39] found left visual-field advantages in adults (aged 25-79) on a nonverbal facial matching task, regardless of age. LEVINE and LEVY [31] demonstrated left hemispace biases in two groups of subjects (aged 5-17 and 70-80) on the same chimeric faces task employed in this study, again. regardless of age. For expression, BOROD et al. [6] demonstrated left-sided facial asymmetry in male subjects (aged 45-75, R= 59.1), who were older than the research subjects typically used in facial asymmetry studies. Thus, there does not appear to be behavioral support for the aging hypothesis when facial processing is

FACIAL

LATERALITY

AND AGING

207

examined. In fact, there is no neuroanatomical evidence to date demonstrating that the right hemisphere deteriorates more than the left hemisphere as a function of the aging process. However, this study did demonstrate left-sided advantages for both the expression and perception of facial emotion. In light of presumed contralateral innervation for facial asymmetry [19] and for chimeric face perception [23,32], our data provide support for right hemisphere dominance in emotion. Although most of the literature supports the role of the right hemisphere in emotional processing (“right hemisphere hypothesis”) [7, 151, there also have been studies suggesting right hemisphere mediation in negative emotion and left hemisphere mediation in positive emotion (“valence hypothesis”) [13, 431. In the current study, a specific analysis was conducted to examine the influence of valence on the facial asymmetry data. The absence of significant Valence by Hemiface interactions in the ANOVA reported above indicates that patterns of hemiface intensity were consistent across positive and negative emotions. Thus. our expression data provide no support for the valence hypothesis. (Our perception data do not address this issue since only one valence, i.e. positive, was studied.) This study also addressed the issue of whether there are changes in the intensity of facial expression as a function of age. As reported above, there was a significant interaction between Age Group and Emotion. It occurred to us that this interaction might be mediated by intensity differences due to facial wrinkles and folds in the resting or neutral face as a function of age, particularly since slow-sign vehicle changes have been noted in older faces [35]. It also is possible that the overall finding of left-sided facial asymmetry might be confounded by morphological or peripheral features of the resting face, as suggested by EKMAN [20] and FRIDLUND er al.[22]. To control for these possible biases, intensity ratings for the neutral expression of indifference were examined. A 2-way ANOVA (Age Group, Hemiface) yielded significant effects for Age Group (F= 11.47; d.f. = 2, 87; P-cO.001). Hemiface (F=4.50; 1,87; P, o/ 2x. Koc~t.. K. M. Age-related changes In cognitive abilities and hemispheric specialization. Lrfr-hurtd~,[/,~rr\. J. HI.KKOZ (EdItor) Academic Press. New York. 1980.

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AGING

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29. LADAVAS.E. The development of facedness. Cortex 18, 535-545. 1982. 30. LEVIN, H. S., HAMSHER, K. DE S. and BENTON,A. L. A short form of the Test of Facial Recognition for clinical use. J. Psycho/. 91, 223-228, 1975. 31. LEVIPIT, S. C. and LEVY, J. Perceptual asymmetry for chimeric faces across the life span. Brawn Cognit. 5. 291-306, 1986. 32. LEVY,J., HELLER,W., BANICH,M. and BURTON,L. Asymmetry of perception in free viewing of chlmeric faces. Brain Cognit. 2, 409%419, 1983. 33. LYNN, J. G. and LYNN,D. R. Smile and hand dominance in relation to basic modes of adaptation. J. Ahnorm. Sot. Psycho/. 38, 25G276, 1943.

34. MALATESTA, C. Z. and IZARD,C. E. Introduction: conceptualizing emotional development in adults. In Emorion in Adult Lkwelopment, C. Z. MALATE.VAand C. E. IZARD(Editors). Sage Publications. California. 1984. 35. MALATESTA, C. Z., IZARD,C. E., CULVER.C. and NICOLICH.M. Emotion communication skills in young. middle-aged. and older women. Psychol. Aging 2, 193-203. 1987. 36. MATTIS,S. Mental status examination for organic mental syndrome in the elderly patient. In Geriatric Psychology, L. BELLAKand T. B. KARASU(Editors). Grune & Stratton, New York. 1976. 37. NEWTON,N., LAZARUS,L. W. and WEINBERG, J. Aging: biopsychosocial perspectives. In NormolirJ and the L!fe Cycle, D. OFFERand M. SABSH~N (Editors). Basic Books, New York, 1984. 38. OBLER,L. K.. ALBERT,M. L., GO~DGLASS,H. and BENSON,D. F. Aphasia type and aging. Brai, Lang. 6. 318-322, 1978. 39. OBLER,L.. WOODWARD, S. and ALBERT,M. Changes in cerebral lateralization in aging? Neuropsychologia 22. 235-240, 1984. 40. PORAC,C., COREN,S. and DUNCAK,P. Life-span age trends in laterality.

J. Geront. 35, 715-721, 1980. 41. I&GE, W. H., METTER,E. J. and WILLIAMS,M. Y. Age and hemispheric asymmetry in nonverbal tactual memory. Neuropsychologia 18, 707-710, 1980. 42. ROSEN,J. L. and NEUGARTEP;, B. Ego functions in the middle and later years: a thematic apperception study of normal adults. J. Geront. 15, 62-67, 1960. 43. SACKEIM,H. and GUR. R. C. Lateral asymmetry in intensity of emotional expression. Neuropsycholoyia 16, 473481,197s. 44. SACKEIM.H., WEIMAN,A. L. and FORMAN,B. D. Asymmetry of the face at rest: size, area, and emotional

expression. Cortex 20, 165-178, 1984. 45. SILBERMAN, E. K. and WEINGARTNER, H. Hemispheric lateralization of functions related to emotion. Brain Cognit. 5, 322-353, 1986. 46. STRAUSS,E. and MOSCOVITCH, M. Perception of facial expressions. Brain Lang. 13, 308-332, 1981. 47. TUCKER, D. M. and FREDERICK,S. L. Emotion and brain lateralization. In Handbook of Social Psychophysiology, H. L. WAGNERand A. S. R. MANSTEAD (Editors). John Wiley, New York. 1989. 48. WEBER,S. Facial asymmetry in the expression of emotion in infants. Doctoral dissertation. New York University, 1983. 49. WECHSLER, D. WAIS-R Manual. Psychological Corporation, New York, 1981. 50. ZUNG, W. A self-rating depression scale. Archs gen. Psychiat. 12, 63-70, 1965.

Lateralization for the expression and perception of facial emotion as a function of age.

In order to test the hypothesis of right hemisphere changes with age, this study examined lateralization for facial emotion in young, middle-aged, and...
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