Decreased perceptual sensitivity to emotion-evoking stimuli in depression

127

Psychrarry Research, 5 1:127-I 38 Elsevier

Decreased Perceptual Sensitivity Stimuli in Depression Bruce E. Wexler, Lawrence Lawrence H. Price

Levenson,

Received

version

January

25, 1993; revised

to Emotion-Evoking

Stephen

received

October

Warrenburg,

5, 1993; accepred

and

October

2.5, 1993.

Abstract. We measured two aspects of emotional response in depressed patients, as a preliminary study of the potential usefulness of such measures for elucidating pathophysiological mechanisms. First we used electromyography to measure the automatic mimicry on an individual’s own face of facial displays of emotion observed on the faces of others. Next we used the fused dichotic listening paradigm to measure selective perception of both positive and negative emotionrelated words as opposed to neutral words. Patients failed to show the normal

facial mimicry of both positive and negative facial displays, despite normal cognitive processing of the stimuli. They also heard significantly fewer positive and negative words on the dichotic tests than did healthy controls. This suggests that depressed patients are hyposensitive to emotion-related stimuli in general. Key Words.

Affective

disorder,

electromyography,

dichotic

listening,

attention.

Medical specialties other than psychiatry rely heavily on objective assessments of basic physiological processes to guide diagnosis, and to help select and monitor treatments. Such measures range from relatively simple measures of pulse, blood pressure, and temperature to more technology-dependent assessments. In psychiatry, development of similar procedures has been slowed by difficulty both in identifying clinically relevant physiological processes and in developing objective measures of those processes. Emotion plays a central role in normal function. Emotional reactions are an important factor determining the selection of behavioral options, and emotional state exerts strong effects on cognitive functions such as perception and memory, as well as on overall level of activity. Emotion is equally central in psychiatric illness. Psychiatric illnesses are often referred to as emotional disorders, and specific disturbances in affect figure prominently in formal diagnostic criteria. Objective assessment of aspects of emotion would seem therefore to be of potential value in diagnosis and in monitoring treatment.

Bruce E. Wexler, M.D., is Associate Professor, Department of Psychiatry, Yale University School of Medicine and Connecticut Mental Health Center. Lawrence Levenson, M.D., is Assistant Clinical Professor, Department of Psychiatry, Yale University School of Medicine. Stephen Warrenburg, Ph.D., is Research Scientist, International Flavors and Fragrances, Inc., Union Beach, NJ. Lawrence H. Price, M.D., is Associate Professor, Clinical Neuroscience Research Unit, Ribicoff Research Facilities, Yale University. (Reprint requests to Dr. B. Wexler, Dept. of Psychiatry, Yale University, 34 Park St., New Haven, CT 06519, USA.) 0165-1781/94/$07.00

@ 1994 Elsevier Science Ireland

Ltd.

128 Over the past decade, researchers in psychology have developed measures of physiological processes that are fundamental parts of emotional response. Change in facial expression is one, with emotion-specific expressions contributing to the perception, expression, and intensity of emotional states. These facial displays seem to be consistent across species (Darwin, 1872), across cultures (Ekman, 1972), and in congenitally blind individuals who have never actually seen them (Charlesworth and Kreutzer, 1973). The intensity of such expressions can be quantified by recording electrical activity in the facial muscles (electromyography, EMG) that either furrow the brow in a frown (corrugator muscles) or raise the sides of the mouth in a smile (zygomatic muscles) (Schwartz et al., 1976a, 1976b; Cacioppo et al., 1986, 1988). Additional physiological processes regulate conscious awareness of emotion-laden stimuli. When dichotic listening techniques (described below) are used, it is possible to evaluate automatic and unconscious perceptual tropisms toward or away from emotionally charged stimuli (Altemus et al., 1989). The present study represents a preliminary investigation of two aspects of emotional reactivity in depressed patients. We chose depressed patients for our initial studies because disorders of emotion appear so central in depression. We chose two physiological measures-facial muscle electrical activity and selective perception of emotion-laden words-based both on our technical familiarity with the measures and on data suggesting that the processes reflected in these measures were likely to be abnormal in depression. Three previous studies have compared facial EMG activity in depressed patients and healthy control subjects. Two compared patients and control subjects in resting states and found higher activity in the corrugator and zygomatic muscles in the patients (Carney et al., 1978; Greden et al., 1986). These EMG data do not suggest an exaggerated negative (corrugator) facial display, but rather an emotionally nonspecific increase in muscle activity. Two studies compared patients and control subjects during periods of self-generated positive and negative affective imagery. Both found that patients failed to show the selective zygomatic region activation seen in healthy subjects with positive imagery (Schwartz et al., 1976~7; Greden et al., 1986). One study found that patients also failed to show the normal selective corrugator activation with negative imagery (Greden et al., 1986) but the other study found similar corrugator activation in patients and control subjects with negative imagery (Schwartz et al., 1976a). In the present study, we were particularly interested in response to emotion-laden cues. Use of self-generated imagery to provide such cues, however, is complicated by potential differences between patients and control subjects in the degree to which they create such internal stimuli. To avoid this problem, we used a standard set of external emotional stimuli. We chose a set of photographs of actors with posed happy, sad, or neutral facial expressions. The particular set of photographs was created for use as experimental stimuli, and extensive previous standardization trials have demonstrated that each picture is essentially universally rated as belonging in the category in which it is placed (Ekman and Friesen, 1976). A previous study with these same stimuli demonstrated that healthy subjects show a selective increase in zygomatic region activity when they view a happy face and a selective increase in

129 corrugator region activity when they view a sad face (Dimberg, 1982). This rapid and automatic EMG response is a measure of perceptual sensitivity to the emotional aspects of the facial stimuli. Our second measure, perceptual sensitivity to emotion-evoking words, is based methodologically on our previous research with fused, rhymed, single-response dichotic listening tests (Wexler and Halwes, 1983; Wexler et al., 1986). In these tests, two words differing from one another only in their initial consonants are presented simultaneously, one to each ear. The initial consonant of one utterance is crossspliced onto the final portion of the other so that the two words are actually identical save for the first consonant. The degree of temporal and auditory spectral overlap that results can be so great that the members of each dichotic pair fuse into a single auditory percept. This means that subjects consciously experience only one word of each stimulus pair. Even when explicitly informed of the nature of these stimuli, subjects are unable to distinguish reliably the fused dichotic pairs from simple binaural presentations of a single stimulus (Repp, 1976), and they are unable to identify selectively the words presented to one ear or the other (Wexler, unpublished data). In this experiment, we used newly constructed dichotic pairs in which one word was previously rated as being emotionally neutral while the other was previously rated as evoking either a positive or negative feeling. Thus, on each trial, the word directed to one ear is neutral, while the word directed to the other generally evokes a positive or negative feeling. Bonanno and Wexler (1992) have shown that subjects identified only one word from each of these stimulus pairs even when told that they would receive two different words on each trial. In the test itself, subjects are simply told to indicate what word they hear on each trial and are not told that they will actually be receiving different words in their two ears at the same time. Sometimes they report hearing the neutral word from the stimulus pair, while other times they report hearing either the positive or negative word from the pair. Emotional proclivity indices (EPI) are calculated by determining the proportion of positiveneutral trials on which the positive word is the one heard or the proportion of negative-neutral trials on which the negative word is the one heard. A possible association between these proportions and mood state is suggested by previous studies showing that most women hear fewer positive words during premenstrual than during postmenstrual periods and that the degree of this change is greater in women who report more premenstrual dysphoria (Altemus et al., 1989).

Methods Subjects. Facial EMG was recorded in 28 patients (26 men, 2 women) at the West Haven Veterans Administration Medical Center who met DSM-III-R criteria (American Psychiatric Association, 1987) for major depressive disorder (MDD) as determined by an attending psychiatrist (L.L.) based on chart review and interview. Fifteen were outpatients (median score on the Hamilton Rating Scale for Depression [Hamilton, 1960]= 17, range = 7-32) and 13 were inpatients (median Hamilton score = 21, range = 10-37). They ranged in age from 27 to 68 with a median of 54.5 years. None had evidence of significant medical or neurological illness by history or on physical and laboratory examination. None met criteria for another primary axis I disorder or for substance abuse within the preceding 6 months according to

130 DSM-ZZZ-R. All were able and willing to give informed voluntary consent to participate in the study. Thirteen patients were not receiving any psychotropic medications at the time of testing, four were receiving only anti-anxiety agents, four were receiving neuroleptics either alone or in combination with other agents, and seven were receiving antidepressants either alone or with anti-anxiety agents. Twenty-eight paid volunteers (14 men, 14 women) who responded to advertisements served as control subjects. The volunteers ranged in age from 18 to 74 years (median = 26). None had a history of neurological or psychiatric illness, including substance abuse disorder, based on screening with the Schedule for Affective Disorders and Schizophrenia-Lifetime version (Endicott and Spitzer, 1978). Dichotic tests were administered to 18 patients (5 men, I3 women) who were hospitalized on the Clinical Neuroscience Research Unit at the Connecticut Mental Health Center and met DSM-III-R criteria for MDD as determined by an attending psychiatrist (L.P.) based on chart review and repeated clinical interviews (median Hamilton score = 35, range = 20-50). They ranged in age from 19-69 with a median of 41 years. None had evidence of significant medical or neurological illness by history or on physical and laboratory examination. None met criteria for another primary axis I disorder or for substance abuse within the preceding 6 months according to DSM-ZZZ-R. All were able and willing to give informed voluntary consent to participate in the study. All had been drug free for at least 2 weeks in the hospital before testing. Twenty-seven paid volunteers (9 men, 18 women), screened by an attending psychiatrist for psychiatric or neurologic illness or current use of prescribed or illicit drugs with central nervous system effects, served as healthy control subjects. They ranged in age from 24 to 45 with a median of 35 years.

Facial EMG. Facial EMG was recorded while subjects sat in a padded armchair in a quiet, dimly lit room. Recordings were made before and while stimulus slides were presented by a slide projector hidden from view by a rear projection screen. Subjects were told that they would see pictures of people’s faces, each for a few seconds, and would be asked later to identify the faces they had seen. They were instructed to sit quietly and look at each face. Recording electrodes were placed over the right and left corrugator and zygomatic regions, with the cheekbones, comers of the mouth and eyebrows, and creases on the forehead being used as landmarks. Dummy electrodes were placed on the right and left forearms to draw subjects’ attention away from their faces. Subjects were told that the electrodes would measure physiological aspects of information processing. Slide presentations did not begin until successive l-minute averages of EMG activity were within 10% of one another, indicating that subjects had acclimated sufficiently to the testing experience to be at a reasonably stable baseline. Ten happy, 10 sad, and 10 neutral faces from the collection of Ekman and Friesen (1976) served as stimuli. During the first half of the testing sessions, blocks of five happy, five sad, and five neutral faces were presented with the order of the blocks counterbalanced across subjects. After a 5-minute rest period, the remaining slides were presented in three similar blocks, with the blocks in the same order as in the first half. Slides were gradually illuminated (fade in) during the first 1.5 seconds of presentation to minimize the physiological effects of abrupt changes in illumination. They were then exposed at full intensity for 9 seconds, before fading out over 1.5 additional seconds. There was a 12-second interstimulus interval. The EMG activity was averaged for successive 2-second periods beginning with the initial fade-in period. Activity of the right and left corrugator and zygomatic muscles was recorded with Beckman miniature Ag/ AgCl bipotential electrodes affixed in pairs over the left and right corrugator and zygomatic regions using a Biolab from Stoelting-Cyborg (Schwartz et al., 1976~). (Although we will hereafter refer to activity of the corrugator or zygomatic muscles, it should be understood that recordings are of activity in these muscle regions and may include some contributions from neighboring muscles.) Interelectrode impedance was reduced to G 7,000 ohms by briskly rubbing Redux paste into the electrode area. EMG was sampled at 100 samples/second with filtering cutoffs at 1 and 100 p.rV, and recorded on-line by an Apple II

131

microcomputer. The raw EMG activity throughout the entire test session for each subject was inspected for artifacts in the form of anomalous bursts of activity (e.g., grimaces), significant and sustained shifts in baseline levels indicative of increased electrode impedance, or marked variability of EMG recordings suggesting electrical instability of the recording electrodes. Trials that were determined to have significant artifact contamination were discarded. One patient and one control subject were dropped from the data set because of extensive artifact contamination, and two patients and one control subject were dropped from the analyses of overall zygomatic activity throughout the testing session for the same reason but included in all other analyses. Preliminary analyses revealed that there were no consistent differences among the five slides in each group of positive, negative, or neutral slides, and there were no consistent differences between the first and second halves of the testing sessions. Consequently, subsequent analyses considered all 10 slides of each affect type together. Visual inspection of the data suggested that the affect-specific responses were greatest during the first 4 seconds of slide exposure for both patients and control subjects. Subsequent analyses therefore used only data from this period and from a comparable 4-second period immediately before the onset of each slide. Since the patient and control groups in the EMG study differed substantially with regard both to age and gender, preliminary analyses were also done to evaluate the relationship between these variables and EMG responsivity. Correlations were nonsignificant between age and the extent of EMG responsivity (the absolute value of the difference between muscle activity during the 4 seconds before each slide presentation and the first 4 seconds of viewing each slide) in both patients and control subjects for both corrugator and zygomatic regions. Similarly, differences between male and female control subjects were nonsignificant for either corrugator or zygomatic responsivity. At the conclusion of the slide presentation and EMG recording protocol, a recognition test of the stimuli was given. Thirty slides were presented, and subjects were asked to indicate after each whether it had been previously presented. Fifteen of these slides had been previously presented, while the 15 others were different actors with posed expressions of one of the three test emotions (happy, sad, or neutral). Dichotic Tests of Perception of Emotion. Two different dichotic listening tests were used, a positive-neutral and a negative-neutral test. In previous research, one word in each pair of the positive neutral test had been consistently rated by a group of young adults as being associated with positive feelings (Wexler et al., 1986). The other word in each pair had been rated as emotionally neutral. One word in each pair of the negative-neutral test had been rated as being associated with negative feelings, while the other was neutral. Words in each pair differed from one another only in their initial consonants (e.g., fun-ton, kill-till). Both tests were made up of 11 different stimulus pairs and contained a total of 88 trials. The lists of actual stimulus pairs have been published elsewhere (Altemus et al., 1989). Copies of the test tapes are available from B.E. Wexler. The positive, negative, and neutral words did not differ significantly from one another in frequency of usage (Bonanno and Wexler, 1992). Test tapes were made at Haskins Laboratories in collaboration with Terry Halwes, Ph.D. Digital recordings were made of each word, spoken by a male voice. The initial consonant portion of one member of each pair was cross-spliced onto the vowel-final consonant portion of the other member on the Haskins Laboratories DDP 224 Computer System, making the members of each pair actually identical save for the initial consonant. This high degree of auditory spectral overlap between the two words in each pair, together with their precise temporal alignment, causes them to fuse into a single auditory percept. Subjects were not told that they would receive two different inputs on each trial, and were consciously aware of hearing only one. It was therefore possible to determine how often subjects heard the emotionevoking words as compared with the neutral words. This was quantified in an emotional proclivity index (EPI) by subtracting the number of neutral words heard from the number of positive (or negative) words heard and dividing the difference by the sum of the two. Tapes were played on a Nakimichi cassette recorder, and stimuli were delivered through

132 matched pairs of TDH-39 earphones. Calibration tones at the beginning of each tape were balanced to minimize channel effects. Earphone assignments to ears were reversed after the first and third quarters of each test to balance for any remaining channel differences. Subjects received simple binaural presentations of each stimulus one at a time, as well as practice dichotic trials, before each test. This ensured that subjects could identify each stimulus, minimized the impact of word-frequency differences between the members of each pair, and familiarized subjects with hearing dichotic stimuli. Subjects indicated the word they heard by marking it on a list of four choices consisting of the two words from the dichotic pair and two foils that differed from the stimuli only in their initial consonants. Both patients and control subjects correctly identified one (and only one) word on essentially all trials.

Results Facial EMG. An initial analysis of variance (ANOVA) was carried out to determine whether control subjects showed the expected differences in facial muscle response when they viewed happy and sad faces. Change in muscle activity from the 4 seconds preceding each slide to the first 4 seconds of viewing each slide served as the dependent measure. Muscle region (corrugator vs. zygomatic), affect (happy vs. neutral vs. sad), and side (right vs. left) served as within-subject factors. The expected muscle X affect interaction proved significant (F= 3.68; df = 2, 52; p = 0.03). As evident in Fig. 1, corrugator activity increased when subjects viewed sad faces and decreased when they viewed happy faces, while the reverse was true for zygomatic activity. Main effects of muscle, affect, and side were all nonsignificant. The analysis of primary interest was then conducted to determine whether depressed patients showed the normal facial EMG response to the emotion-evoking faces. As evident in Fig. 1, patients failed to show the normal muscle X affect interaction (F = 0.34; df= 2, 52; p = 0.71). Main effects of muscle, affect, and side were nonsignificant. While the muscle X affect interaction was significant as expected in the control subjects, and did not approach significance in the patients, direct statistical comparison of the two groups did not yield a significant group X muscle X affect interaction. To ensure that depressed patients “took in” the visual information from the slides to the same extent (even if not in the same way) that healthy control subjects did, performance of the groups on the recognition test was compared. Both groups did well on this test, with patients correctly identifying on average 13.4 of the 15 slides that had been presented during the EMG recording, and control subjects identifying on average 14.1 of the 15. Both groups had average false-positive rates of < 0.5 out of a possible 15. Previous studies reported greater baseline levels of both corrugator and zygomatic activity in depressed patients than in healthy control subjects (Carney et al., 1978; Greden et al., 1986). To evaluate the possibility of a generalized increase in facial muscle activity in patients as compared with control subjects, we compared corrugator and zygomatic activity in the two groups before the presentation of any stimuli, during the interstimulus periods, and during stimulus presentation (Fig. 2). Corrugator activity proved higher in the patients throughout all periods (F = 5.5 1; df = 1, 52; p = 0.02) and there was a similar trend for zygomatic activity (F = 3.40; df = 1, 46; p = 0.07). These differences raised the possibility that the absence of

133

emotion-specific EMG changes in the patients was due to the fact that patients had pathologically high tonic levels of muscle activity that precluded stimulus-dependent responsivity. For both patients and control subjects, however, the correlations between prestimulus corrugator activity and stimulus-related corrugator responsivity were nonsignificant. Both groups showed positive correlations between prestimulus zygomatic activity and zygomatic responsivity (significant in the control subjects and nonsignificant in the patients). Thus, it seems unlikely that the absence of emotionspecific responsivity in patients is due to their generally elevated levels of EMG activity.

Fig. 1. Change in electromyographic activity over the corrugator and zygomatic regions during the first 4 seconds of viewing slides vs. the 4 seconds before slide presentation 25 20 15 r

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134

Fig. 2. Average corrugator and zygomatic actvity in healthy control subjects and depressed patients while resting before any slide presentations, between slide presentations, and while viewing slides

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Perception of Emotion-Evoking Stimuli. Patient and control EPI scores were compared in an ANOVA with diagnosis (depressed vs. healthy) as a betweensubjects factor and affect (positive test EPI vs. negative test EPI) as a within-subjects factor. The main effect of group was significant (F= 12.81; df = 1,43;p < O.OOl), as patients heard fewer positive words (t = 3.49, df = 43, p = 0.001) and fewer negative words (t = 2.53, df =43,p = 0.01) than healthy control subjects (Fig. 3). Neither the main effect of affect nor the interaction between affect and diagnosis was significant.

135 Fig. 3. Selective perception of positive as opposed to neutral words, and negative as opposed to neutral words, in healthy control subjects and depressed patients 0.31’0 =UG a:ir %!!5X- o- e {$$

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Discussion The primary finding of the present study is that depressed patients showed abnormal responses to both positive and negative emotional cues. Abnormalities were noted in two quite different aspects of emotional responsivity-facial EMG and conscious awareness of emotion-related stimuli-and two quite different types of cues-one visual and nonverbal, the other auditory and verbal. Similar findings in such different response measures, and in response to such different cues, support the contention that the abnormality is in processes of emotion instead of in some particularity of one response system or one type of stimulus. The automatic and largely, if not entirely, unconscious nature of both responses makes it unlikely that differences in motivation or effort contributed to the differences between patients and control subjects. Furthermore, since depressed patients accurately identified the stimuli on nearly all trials on both the visual and auditory tasks, and in this regard did not differ significantly from healthy control subjects, it is more difficult still to attribute the decreased responsivity to emotion-evoking stimuli as failure to attend or lack of involvement in the tasks. The study is limited somewhat, however, by differences between patients and control groups in gender mix, and between the two groups of depressed patients in symptom severity. One way to view the findings is that patients were hyporesponsive to both negative and positive emotionevoking stimuli. This suggests that many depressed patients suffer from being disconnected from environmental, emotion-evoking cues. An internal sense of emptiness could result, as indeed some patients complain. Since the right hemisphere appears to play a specialized role in identifying the emotional

136 nature of stimuli (Gainotti, 1983; Ley and Strauss, 1986; Bryden and MacRae, 1989), these findings can be seen as consistent with previous suggestions of a dysfunction of that hemisphere in some types of depression (Flor-Henry, 1976; Tucker et al., 1981; Bruder et al., 1989). In fact, Kinsbourne and Bemporad (1983), in a detailed examination of the possible relationships between hemispheric specialization of normal functions and the pathophysiology of depression, suggested that in one subtype of depression “associated with right (posterior?) lesions, emotional responses are reduced or absent and the emphasis is on an internal emptiness.” An alternative, qualitative view of the EMG findings is that patients showed increased corrugator and decreased zygomatic responses (the “sad” response) when they viewed happy and neutral as well as when they viewed sad faces. There is, however, no indication of greater “sad” responses when they viewed sad faces (i.e., no discrimination among the types of faces viewed). Furthermore, on the dichotic test, depressed patients were clearly subsensitive to the negative words, a response that does not fit nicely with interpretation of the EMG findings as a general tendency to respond to everything negatively. With regard to the dichotic tests, the low EPI score on the positive-neutral test raises the possibility of an actual avoidance of positive stimuli rather than simply a loss of their normal salience. Such a process might also be evident in the EMG, where patients seemed to differ most dramatically from control subjects in showing a marked decrease instead of the normal increase in zygomatic activity when viewing smiling faces. A secondary finding in the present study was that depressed patients showed a tonic increase in both corrugator and zygomatic activity, as compared with healthy control subjects. This is consistent with two previous reports (Carney et al., 1978; Greden et al., 1986). In one, patients were drug-free for lo-14 days before testing, suggesting that the increase in EMG is not due to medications (Greden et al., 1986) although further studies are needed for a full evaluation of this possibility. The tonic increase in corrugator and zygomatic activity is also consistent with earlier reports of a general increase in tension of the body muscles in depression (Whatmore and Ellis, 1959, 1962; Goldstein, 1965). Our findings suggest a number of future studies. First, a study should be done in which both EMG and dichotic listening measures of responsivity are given to the same patients to determine how closely the two abnormalities are linked. Second, both measures should be evaluated before and after treatment, to determine whether they change with or predict clinical recovery. Third, the possibility that decreased responsivity to emotion-evoking stimuli marks a pathophysiologically distinct subgroup of depressed patients should be evaluated by comparing patients with higher and lower degrees of responsivity on other measures. These might include variables such as clinical course or family history on which depressed patients have been shown to differ from one another, or variables such as cerebral laterality, serum testosterone, the dexamethasone suppression test, the thyroid stimulating hormone response to thyrotropin releasing hormone, the growth hormone response to clonidine, or levels of y-aminobutyric acid in cerebrospinal fluid-measures on which some but not all depressed patients have been shown to differ from healthy control subjects.

137

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