Hemispheric lateralization of emotions: Absence of electrophysiological arguments

Physiology & Behavior, Vol. 40, pp. 215--220.Copyright©PergamonJournals Ltd., 1987. Printed in the U.S.A.

0031-9384/87 $3.00 + .00

Hemispheric Lateralization of Emotions: Absence of Electrophysiological Arguments L . C O L L E T 1 A N D R. D U C L A U X

Laboratoire de Physiologie sensorielle, Centre Hospitalier L y o n - S u d 69310-Pierre-B~nite , France R e c e i v e d 29 J u l y 1986 COLLET, L. AND R. DUCLAUX. Hemispheric lateralization of emotions: Absence of electrophysiological arguments. PHYSIOL BEHAV 40(2) 215-220, 1987.--EEG lateralization was examined during happy and sad emotional expression in 24 subjects. Happy and sad emotional states were induced by asking subjects to mentally review previously shown film-sequences. Our results failed to replicate those of previous studies, in that they showed no frontal alpha lateralization as a function of emotion. The authors discuss the literature and suggest caution before asserting the existence of electrophysiological arguments in favor of lateralization of emotions in humans. Emotions

EEG asymmetry

Laterality

Hemispheric function

S E V E R A L neuropsychological and physiological studies suggest that the left hemisphere is particularly involved in the expression of happy emotions, in right-handed subjects, and the fight hemisphere in that of sad ones. The question is, however, a subject of controversy. In neuropsychology, cases of pathological laughing are more frequently associated with right hemisphere damage, whereas pathological crying is more frequently associated with left hemisphere damage. Likewise, right hemispherectomy is associated with a euphoric mood [9]. Unilateral injections of sodium amobarbitol have shown that, when the fight hemisphere is barbiturated, most subjects show a euphoric reaction, whereas for the left hemisphere most show a reaction of sadness. Now, this emotional reaction of sadness might, according to Hirschmann and Safer [8], be explained in terms of aphasia, often associated with left hemisphere damage: it might be a manifestation of the loss of capacity for verbal communication. Thus, from a neuropsychological point of view, simple observation of hemispheric deficits is insufficient grounds to affirm that one hemisphere is more specifically the site of some particular emotion. The psychological approach is to measure certain physiological parameters, thought to be dependent on one or other hemisphere, under induced emotional response. The literature is based on three such measurements: (1) facial electromyography (EMG), (2) electro-oculography (EOG) and (3) electroencephalography (EEG). EMGs have shown that several facial muscle systems are involved in emotional expression [10]. The various mental

images associated with happy or sad situations are also associated with various patterns of facial muscle activity. Thus, a happy feeling reduces the corrugator EMG, whereas sadness augments it. Conversely, happy feelings augment the zygomatic EMG, whereas sadness reduces it [5, 11, 12, 14]. Schwartz et al. [13] have used these electromyographic measurements to study the presence of a facial asymmetry in response to induced emotions. They showed the existence o f lateralized zygomatic responses: greater right E M G activity in response to happy emotional evocations, and greater left activity in response to sad ones. We can interpret these results in terms of a predominance of fight hemispheric activity for sadness and of left activity for happiness. However, such an interpretation would be open to question, as the same study failed to show lateralization of corrugator muscle responses. EOGs have followed the first lateral ocular movement after emotional imagery: according to A h e m and Schwartz [1] happy emotions tend to give rightward lateral eye movements, whereas sad emotions tend to give more leftward movements. However, since Hatta [6] failed to replicate these results, they do not justify the assertion of an emotional hemispheric asymmetry. There have been few E E G studies concerning cerebral lateralization of emotions. Davidson et al. [2] showed that relative to a vertex reference the frontal areas are associated with a greater relative left during positive versus negative emotional state in the alpha-band; Davidson and Fox [3] have extended these affect lateralization findings to infants. These E E G studies

1Requests for reprints should be addressed to L. Collet, Hbpital Edouard Herriot pavilion U, Place d'Arsonval, 69374-Lyon C(~dex 08, France.

215

3 12 0 8 1

-0.0332 -0.5527 0.2353

107 NS

S

1 8 1 9 5

0.066 -0.195 0.426

54 p<0.01

-0.0187 -0.2778 0.3851

-0.0492 -0.363 0.106 5 10 I 4 4

H

P3--P4 S

7 7 1 8 1

1

2 11 0 8 3

-0.002 -0.143 0.157

H

140 NS

S

2 9 1 10 2

0.0044 -0.28 0.146

C3-C4

2 9 2 9 2

0.0074 -0.111 0.174

H

136 NS

S

1 8 2 9 4

0.0159 -0.111 0.152

F3--F4

12 6 0 4 2

-0.0996 -0.617 0.2062

H

128 NS

S

9 8 0 7 0

-0.097 -0.613 0.0994

T5-T6

2 9 4 7 2

0.0035 -0.126 0.253

109 NS

4 5 1 8 6

0.0108 -0.30 0.176

0.0212 -0.149 0.173 1 9 0 8 6

H

S

120 NS

S

1 8 2 8 5

0.0116 -0.247 0.20

P3-P4

6 6 1 10 1

-0.0218 -0.268 0.149

H

129 NS

S

5 10 2 6 1

-0.0654 -0.909 0.126

C3-C4

0 10 4 8 2

0.0152 -0.0967 0.223

H

116 NS

S

3 7 3 9 2

-0.0005 -0.222 0.150

F3--F4

1 6 2 5 10

0.0557 -0.106 0.266

H

117 NS

S

2 5 1 5 11

0.0792 -0.114 0.286

T5-T6 H

3 10 1 8 2

92 NS

S

11 3 2 7 1

-0.0871 -0.4762 0.1429

S

80 p <0.05

2 7 3 7 5

0.0155 -0.175 0.186

T3-T4

-0.0135 -0.21 0.22

E a c h condition is defined for each subject according to an E M G criterion. Higher n u m b e r s indicate greater relative right side activation. m: mean; min: m i n i m u m value; max: m a x i m u m value; N: n u m b e r o f subjects; LRS: laterality ratio score.

m min max N: <-0.10 [ - 0 . 1 0 , 0] 0 [0, 10l >0.10 Wilcoxon

H

O 1-O2

2

8 6 1 5 4

THETA LATERALITY RATIO SCORES BY CONDITION BETWEEN SYMETRICAL SCALP ELECTRODES

TABLE

H

T3-T4

-0.0318 -0.219 0.2295

E a c h condition is defined for each subject according to an E M G criterion. Higher n u m b e r s indicate greater relative right side activation. m: mean; min: m i n i m u m value; max: m a x i m u m value; N: n u m b e r o f subjects; LRS: laterality ratio score. H: happy; S: sad; The position of the electrodes is according to the International s y s t e m .

m min max N: <-0.10 [ - 0 . 1 0 , 0] 0 [0, 10] >0.10 Wilcoxon

H

O 1-O2

TABLE ALPHA LATERALITY RATIO SCORES BY CONDITION BETWEEN SYMETRICAL SCALP ELECTRODES

4 10 1 6 3

-0.0093 -0.196 0.154

H

144 NS

114 NS

S

2 9 1 9 4

-0.0029 -0.333 0.164

S

6 8 1 6 3

-0.0285 -0.274 0.207

T l-T2

-0.0057 -0.235 0.1845

H

T l-T2

r-'

> Z

©

W p

max

m rain

m rain max W P

22 NS

0.0168 -0.0638 0.111

0.007 -0.0909 0.0927

0.0361 -0,200 0.176

H

29 NS

S 0.0396 -0.158 0.200

P3-P4 S

H

S 0.0612 -0.195 0.387

O 1-O2

-0.0417 -0.2778 0.3851

H

10 p <0.05

-0.0183 -0.1140 0.1060

S

P3-P4

25 NS

-0.0296 -0.5527 0.2353

H

01--02

31 NS

S -0.0308 -0.121 0.126

C3-C4

-0,329 -0.268 0.0769

H

21 NS

TABLE 4

0.025 -0.111 0.1091

H

S 0.0108 -0.111 0.101

F3.-F4

31 NS

S 0.0058 -0.222 0.101

F3-F4

0.0164 -0.0967 0.0989

H

H

20 NS

S 0.1097 -0.108 0.286

T5-T6

0.0793 -0.071 0.266

H

33 NS

S -0.0708 -0.345 0.0994

T5-T6

-0.0979 -0,4965 0.2062

T H E T A L A T E R A L I T Y SCORES IN M A L E S

26 NS

S 0.0189 -0.108 0.146

c3--c4

0.002 -0.1309 0.1090

H

TABLE 3 A L P H A L A T E R A L I T Y SCORES IN M A L E S

12 NS

27 NS

S

-0.0015 -0.175 0.186

S

-0.0835 -0.3302 0.1429

T3-T4

-0.0143 -0.21 0.22

H

0.0152 -0.202 0.2295

H

T3-T4

25 NS

16 NS

S

-0.0448 -0.274 0.207

S

0.0244 -0.0909 0.1640

T I-T2

-0.0023 -0.106 0.132

H

0.0442 -0.1891 0.1845

H

T l-T2

"-d

O

rn

O

Z

N >,

t>, ,...] rn

m

W p

max

min

m

W p

max

rain

31 NS

0.025 -0.149 0.173

0.0006 -0.126 0.253

-0.0106 -0.3000 0.1230

H

33 NS

S

-0.0121 -0.247 0.155

P3-P4 S

H

O 1-O2

0.070 -0.0886 0.426

0.0009 -0.277 0.134 29 NS

-0.0754 -0.363 0.0819

-0.0362 -0.161 0.0732

S

P3-P4 H

30 NS

S

H

O 1-O2

TABLE 5

TABLE

6

39 NS

S

0.0201 -0.0746 0.152

F3-F4

-0.0074 -0.101 0.174

H

32 NS

S

-0.0947 -0.909 0.0765

C3-C4

-0.0124 -0.143 0.149

H

30 NS

S

-0.0058 -0.126 0.150

F3-F4

0.0141 -0.0909 0.223

H

H

0.0534 -0.114 0.250

0.0358 -0.106 0.200 42 NS

S

H

T5-T6

30 NS

S

-0.1191 -0.613 0.0955

T5-T6

-0.101 -0.617 0.159

T H E T A L A T E R A L I T Y SCORES IN F E M A L E S

42 NS

S

-0.0079 -0.280 0.121

C3-C4

-0.0054 0.143 0.157

H

A L P H A L A T E R A L I T Y SCORES IN F E M A L E S

S

15 p <0.05

0.0299 -0.1000 0.153

T3-T4

-0.0127 -0.118 0.101

H

38 NS

S

-0.0902 -0.4762 0.939

T3-T4

-0.0717 -0.219 0.033

H

44 NS

S

-0.0146 -0.111 0.108

T1-T2

-0.0152 -0.196 0.154

H

34 NS

S

-0.0259 -0.333 0.121

T l-T2

-0.0480 -0.235 0.155

H

X

t"3 t" >

Z

~.q

('3 © t"

oo

HEMISPHERIC LATERALIZATION OF EMOTIONS

219

TABLE 7 MEAN CENTROPARIETALALPHA AND TEMPORALTHETA LATERALITYRATIO SCORES BY CONDITION

Happy

Sad

Wilcoxon Matched Pairs Sign Ranked Test

- 0.0138

0.0145

84

<0.06

-0.0044

-0.00715

101

NS

Condition

Centroparietal alpha Temporal theta

p

Each condition is defined for each subject as the mean of the three laterality ratio scores of each emotional induction.

have not included the theta-band (4-8 Hz) and have been restricted to the frontal area. E E G s thus favor the idea of emotional hemispheric asymmetry, whereas the neuropsychological, electromyographic and electro-oculographic evidence is open to question. We thus thought it worthwhile to study the existence of E E G lateralization associated with happy and sad emotional expression, by recordings taken over the whole scalp, on both theta (4-8 Hz) and alpha (8-13 Hz) bands. METHOD

Subjects Twenty-four volunteer subjects, 11 male, 13 female, ages 18-45, except one female 15 years old (mean age=23.6) took part in the study. Subjects were all right-handed with no family history of left-handedness. Handedness was determined by self report.

Procedure We recorded the electroencephalogram (EEG) and left corrugator electromyogram (EMG) from each subject via surface electrodes. After a 5 minute rest period, with eyes closed, subjects watched one of three film sequences (which we shall call " h a p p y , " " s a d " and " n e u t r a l " respectively) on a TV screen. These sequences had been previously selected by the experimenters as inducive of the corresponding emotional states. At the end of the showing, subjects were asked to close their eyes and mentally review the scenes they had just seen and heard with maximum concentration. This mental reviewing was divided into 3 successive 30 second periods. The order of presentation of the happy, sad and neutral film sequences and of the corresponding review periods was determined according to a factorial plan. Each of the 6 possible combinations was experienced by 4 subjects. E E G s and left corrugator EMGs recorded during the review periods were analyzed. Testing time per subject was about one hour.

Measurements Electromyography. Left corrugator muscle E M G was recorded between 2 silver/silver chloride cup-electrodes placed on the left side of the bridge of the nose [5]. The EMG signal was filtered (band pass 10 Hz, 1000 Hz), amplified, corrected and averaged by an E M G 120 biofeedback system apparatus. Average E M G activity was expressed in/xV. We

took measurements for the average EMG for each 30 second review-period for the happy, sad and neutral film sequences. Electroencephalography. Sixteen channels of E E G were recorded simultaneously via electrodes placed on the scalp according to the standard international system: 7 pairs of electrodes placed symmetrically on each side of the head 2 median electrodes; the reference for each electrode was the ensemble of the others. The E E G signal was processed through a Cartovar (Alvar Electronic) apparatus which allowed spectral analysis of the 16 E E G channels. The E E G frequencies under study were the theta (4-8 Hz) and alpha (8-13 Hz) bands. F o r each electrode we took the average power measured in/zV2/sec, over the 30 seconds for each review-period of the happy, sad and neutral film sequences. Film sequences. The film sequences were taped via a video-recorder from television programs and edited so as to give 3 sequences of 5 to 7 minutes each. The " s a d " sequence was taken from a documentary about death by starvation in an Ethiopian refugee camp: the " h a p p y " sequence was taken from a TV comedy program comprising a series of gags. The " n e u t r a l " sequence concerned a journey in Nepal in the Himalayas.

Analysis of Results Our results of the happy and sad periods have been analyzed in two ways: First, for each subject and each emotional induction, we had 3 series of measurements. In order to select, for each induction, the optimal mental reviewperiod in terms of the desired emotional expression, we classified the corrugator E M G activity values. Given that these values are greater the sadder the subject [9] we decided to analyze, for the sad period, only that 30 second period which showed the greatest EMG activity: for the happy period, that which showed the least. Thus, for each subject, we considered 2 periods: one happy, one sad. We then compared E E G laterality ratio scores (calculated as the ratio left-right/left+right power for all 7 electrode pairs) in the alpha and theta ranges for the happy and sad periods. Secondly, only for the laterality ratio scores which showed a significant difference (at 0.05) we have compared the mean of the 3 laterality ratio scores of each emotional induction to study the reliability of the results. Results were analyzed by a non parametric test: the Wilcoxon Matched Pairs Sign-Ranked Test [15].

220

COLLET AND D U C L A U X RESULTS

(1) If we analyze only the periods according to the EMG values, happy-sad comparison of iaterality ratio score showed a significant difference in only 2 cases (Tables 1 and 2). Ca) The laterality ratio score is significantly higher on the right, for " h a p p y " for alpha activity in the centro-parietal areas ( m e a n = - 0 . 0 1 8 7 as against 0.0659, Wilcoxon Test; p<0.01). (b) It is likewise significantly higher on the right for " h a p p y " for theta activity in the mid-temporal areas ( m e a n = - 0 . 0 1 3 5 against 0.0155, p<0.025). (c) Analysis of sex differences showed a significant difference in males for alpha activity in the centro-parietal areas ( m e a n = - 0 . 0 4 1 7 as against 0.0612, Wilcoxon Test; p<0.05) (Tables 3 and 4) and in females for theta activity in the mid-temporal areas ( m e a n = - 0 . 0 1 2 7 as against 0.0299, Wilcoxon Test; p<0.05) (Tables 5 and 6). (2) If we analyze the mean of the 3 periods for each emotional induction (Table 6), the laterality ratio score has a significant tendency to be higher on the right for " h a p p y " for alpha activity in the centro-parietal areas ( m e a n = - 0 . 0 1 3 8 against 0.0145, p<0.06). But it is lower on the right for " h a p p y " for theta activity in the mid-temporal areas (mean= -0.0044 against -0.00715, NS). This last result does not confirm the tendency observed in the first analysis of the results.

DISCUSSION Handedness of the subjects was determined by self report. This is not a precise indication of handedness but the number of subjects in this study and the absence of family history of left-handedness suggest that the results can be analyzed in terms of laterality differences. The two ways of analysis show different statistical results. However, this discrepancy is not surprising: the mean of the three laterality ratio scores of each emotional induction is the mean of emotional expressions of high and low

quality. The results show a statistical tendency (/9<0.06) toward a centro-parietal alpha lateralization and they become statistically significant (p<0.01) when we choose EEG periods according to an EMG criterion. It may be hypothesized that using an objective physiological criterion, we have selected a best EEG emotional expression. Schwartz et al. [14] have demonstrated that females (as compared to males) show greater emotional expression during affective imagery. The analysis of sex differences in our experiment does not show an EEG lateralization more frequent in females although there are differences: males have a centro-parietal alpha difference and females a temporal theta difference. It could also be supposed that the significant difference was a chance phenomenon due to multiple comparisons. All significance levels below 0.05 were shown, although since fourteen measurements are being compared (7 EEG derivation pairs × 2 EEG activities) only significance levels below 0.0036 should be considered as meaningful (Hays [7]). Hence, in our view, this result must be interpreted with caution but may not justify our concluding for an emotional hemispheric asymmetry at the centro-parietal areas. Moreover, we found no difference in alpha lateralization in the frontal areas, contrary to previous findings [2]. The results suggest caution before asserting the existence of electroencephalographic arguments in favor of lateralization of emotion in humans. As we have already seen that the neuropsychological, etectromyographic and electro-oculographic evidence is likewise open to question, there can be said, overall, to be no physiological findings which assert asymmetry in emotional expression.

ACKNOWLEDGEMENTS We wish to thank the Alvar Company which provided the Cartovar apparatus used in this study, and Ilia Pernoud for her contribution.

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