Differences in dichotic listening asymmetries in depression according to symptomatology

Journal of Affective Elsevier

Disorders, 18 (1990) l-9

JAD 00660

Differences

in dichotic listening asymmetries according to symptomatology Jocelyn Wale 1 and Vaughan

in depression

Carr 2

’ Royal Adelaide Hospital, Adelaide, SA, Australia and ’ University of Newcastle, Newcastle, NS W, Australia (Received 25 October 1988) (Revision received 6 April 1989) (Accepted 18 April 1989)

Subjects suffering from major depressive disorder were compared to normal controls on two verbal dichotic listening tasks. Although there were no significant differences between the groups on a task primarily of language perception, significant differences were obtained on a task with an attentional component. Overall performance was lower for the depressed group and ear asymmetry was reduced. Within the depressed group ear asymmetry varied according to symptomatology; withdrawal-retardation was associated with a lack of asymmetry and anxiety with a normal right ear advantage. The results were interpreted in terms of an interaction between affect and attention, and possible underlying mechanisms of cerebral hemisphere function were discussed.

Key words: Depression;

Dichotic

listening;

Symptomatology;

Introduction Research into the possible relationship between psychopathology and atypical cerebral laterality has produced several studies suggesting involvement of the right hemisphere in affective disorders. These investigations have used a range of behavioural techniques for studying hemisphere function including dichotic listening. Despite inconsistencies in the findings, there appears to be a

Address for correspondence: cipline of Psychiatry, University South Wales, 2308, Australia. 0165-0327/90/$03.50

Professor Vaughan Carr, Disof Newcastle, Newcastle, New

0 1990 Elsevier Science

Publishers

Attention

convergence of evidence from dichotic listening data suggesting differences in ear asymmetry according to diagnostic subtype (see Bruder, 1983, for a review). This calls into question the simple hypothesis that affective disorder is associated with a non-specific abnormality in right hemisphere function. On verbal dichotic listening tasks the normal right ear advantage (REA) tends to be enhanced in persons with bipolar disorder (Lishman et al., 1978; Yozawitz et al., 1979) and this can be interpreted as reflecting a disturbance in right hemisphere function leading to a reduced level of responding to left ear items which are projected via the right hemisphere to the left hemisphere for

B.V. (Biomedical

Division)

2

processing. By contrast, patients with unipolar depression have been found to show no REA on dichotic tasks (Moscovitch et al., 1981; Johnson and Crockett, 1982). This finding suggests a decline in left hemisphere function, given the assumption that the normal REA reflects the predominance of the left hemisphere for language processing. However, different interpretations have been offered for the reduced or absent REA found in depression. Furthermore, the finding of increased ear asymmetry with recovery from depression (Moscovitch et al., 1981; Johnson and Crockett, 1982) indicates that reduced ear asymmetry is a transient state and hence any theoretical interpretations must take this into consideration. Moscovitch et al. (1981) found that whereas depressed persons requiring electroconvulsive therapy (ECT) tended to show no REA on a dichotic task, those treated with antidepressant drugs showed normal ear asymmetry. They suggested that the lack of a REA was due to a ‘strongly primed right hemisphere’, with a return to normal asymmetry following unilateral ECT to that hemisphere. Johnson and Crockett (1982) found a similar reduction in ear asymmetry in depressed persons with return to a normal REA following treatment with medication. They proposed that these changes in asymmetry were due to shifts in the relative activity of each hemisphere which, in turn, could be due to: (a) changes in interhemispheric inhibition via the corpus callosum, (b) intrahemispheric changes in response to medication, or (c) shifts in attentional bias or cognitive strategies by which processing capacity is allocated to the cerebral hemispheres. The suggestion of attentional bias is amenable to further investigation if different tasks of lateral asymmetry in processing are used. Tasks which differentiate between language processing and attentional bias may at least begin to clarify the underlying mechanisms which contribute to the processing asymmetries found with depression. The study by Moscovitch et al. (1981) also demonstrated that different groups of depressed subjects may vary in the ear asymmetries obtained with only the more severely depressed (i.e., those treated with ECT) showing a lack of normal asymmetry. Recent papers (Carr and Wale, 1988; Wale

and Carr. 1988) on perceptual asymmetries in schizophrenia and depression reported a reduced or absent REA for unipolar depressives and also for schizophrenic subjects rating high for negative symptoms and low for positive symptoms (hallucinations and delusions). This suggests that both of these disorders may have some process in common, perhaps reflected in the similar phenomenology of psychomotor retardation and negative symptoms, which is reflected in a decreased REA regardless of the primary pathology. Different studies tend to vary in the type of dichotic task used with little concern for the role that such factors as the attention and/or memory demands of the task may play in performance, or the low demonstrated reliability of some dichotic measures. Given the likely importance of attention to performance, task selection with these issues in mind would therefore seem to be just as important to research in this area as are questions of diagnostic subtype or symptomatology. The use of more than one dichotic test with different task demands, carefully chosen for demonstrated reliability, may help to clarify the mechanisms contributing to the perceptual asymmetries found in depression. Similarly, if reliable tasks are chosen according to specific task demands, questions regarding variations in performance according to symptomatology may be pursued. Two dichotic language tasks with demonstrably satisfactory levels of reliability and validity are the Fused Rhymed Words (FRW) test of Wexler and Halwes (1983) and the Dichotic Monitoring (DM) task of Geffen et al. (1978) and Geffen and Caudrey (1981). The former is primarily a language processing task of phonemic discrimination, similar to consonant-vowel syllable tasks in that only the initial stop consonants of each word pair differ. However, the task has been constructed to increase its power by minimising the effects of stimulus dominance and the opportunity for phonetic blend errors to occur. The second task, originally used for research into attention (Moray and O’Brien, 1967) uses phonemically distinct word pairs and has a large attentional component. It requires ongoing attention to a stream of information presented at a relatively rapid rate with the different items of each dichotic word pair being spatially separate. Thus the use of these two tasks

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should enable questions regarding spatial attentional bias and/or left hemisphere language processing to be addressed. Using these two different tasks of lateral asymmetry in performance, the present study examined the ear asymmetries found in persons suffering from depression, and also attempted to determine whether or not changes in asymmetry were associated with particular types of symptomatology. If attentional factors are critical to the performance of depressed persons, then the asymmetries found on the DM task could be expected to vary from those of normals while the FRW scores would not be similarly affected. Alternatively, anomalies in language processing or overall hemispheric functioning should be reflected in both the FRW and the DM results. Subjects and methods Subjects There were 24 subjects (eight male, 16 female) who met DSM-III criteria (American Psychiatric Association, 1980) for major depressive disorder (unipolar). The distribution of diagnostic subtypes was as follows: without melancholia, 17; with melancholia, 3; with psychotic features, 4. Ages ranged from 15 to 63 years (mean = 42.5 years, SD = 16.5). They were matched for age and sex with 24 volunteer control subjects having no known psychiatric or neurological condition, drawn primarily but not exclusively from hospital staff and covering a range of occupations. The depressed subjects were recently admitted in-patients to a short-term psychiatric treatment unit in a general hospital. The clinical condition of each was considered sufficiently severe to preclude out-patient treatment. All subjects were assessed for handedness using the Annett (1970) handedness questionnaire and the distribution of hand preferences for each group did not vary significantly (depressed: 18 right, 2 left, 4 mixed; controls: 19 right, 4 left, 1 mixed). Of the depressed subjects, 83% were free of antidepressant medication; the remainder had been on antidepressant medication for an average of 2.75 days. One third of the depressed group were completely medication-free and, apart from those who had just commenced antidepressant therapy, a further five had

been given a night-time sedative hypnotic, three were on low-dose benzodiazepines, two on a neuroleptic agent and three were taking some combination of these. Subjects were not included if there was a history of recent alcohol or psychoactive drug abuse or neurological disorder. Apparatus Each of the dichotic tasks has been described in detail elsewhere (Geffen et al., 1978; Wexler and Halwes, 1983). The FRW test requires the subject to indicate which word is heard when two words, differing only in the first phoneme, are presented simultaneously one to each ear and fuse so that there is only one perception. Responses for eight lists of 30 word pairs were recorded manually by the test administrator and later entered onto an Apple IIe computer for analysis. The DM task requires the subject to press a response button whenever a target word (‘dog’) is heard. Lists of 120 word pairs containing 20 targets (10 for each ear), phonemic distracters and irrelevant words were presented simultaneously one to each ear at a rate of l/750 ms. Responses and stimuli were recorded on an Apple IIe computer as described by Wale and Geffen (1986) for further analysis. Stimuli for each task were presented using Maico auraldome headphones and a Uher two-channel tape recorder. Programmes were obtained from each of the relevant laboratories where the tests were developed for the scoring and analysis of individual subject results. Procedure The depressed subjects were interviewed and administered all research procedures within 72 h of hospital admission. The Brief Psychiatric Rating Scale (BPRS) (Overall and Gorham, 1962) was administered by one of the authors (V.C.) as part of a larger research study of schizophrenia. The interview on which the BPRS ratings were based was that of the Present State Examination (Wing et al., 1974). The BPRS has previously shown differences in dichotic listening performance in schizophrenic subjects according to symptom rat-. ing (Carr and Wale, 1988). Within 24 h of the clinical assessment, the two dichotic listening tasks were administered. Half of each subject group performed the FRW test prior to the DM test and

4

this order was reversed for the other half of the group. There were rest periods between each of the tasks and whenever the depressed subjects requested a break in the procedure. The tasks were always administered in the afternoon to offset possible effects of diurnal mood variation on the results of the depressed group. Two practice lists preceded the FRW task. The DM test was preceded by a brief test of hearing consisting of two tones which should be heard centrally if hearing is equal in each ear (Geffen et al., 1978) and a shaping procedure consisting of monaural lists. Since audiometric testing was not readily available, subjects were excluded if these preliminary procedures revealed any evidence to suggest reduced hearing in one ear compared to the other. After two dichotic practice lists, four test lists were administered. The hand of response was counterbalanced in a R/L/R/L order, and the headphones were reversed after alternate lists. Results The analysis programme for the FRW test corrects for stimulus dominance (Halwes, 1969) and corrected scores for each ear were used in statistical comparisons. On the DM task, performance between the groups was compared on the percentage of targets detected (i.e., hit rate, HR) and also on the reaction time (RT) to correct responses. Repeated measures ANOVAs, group (2) x ear (2) were carried out on each of these measures. Planned comparisons using f-tests were also done on ear differences for each group to determine whether these accorded with previous research findings. There were no main or interaction effects on the FRW measure. In the DM experiment the control group detected more targets than the depressed group (see Table l), F(l, 46) = 15.02, P < 0.001, and responses over both subject groups were greater to the right ear (mean = 83.8, SD = 13.9) than to the left ear (mean = 78.0, SD = 16.8) F(1,46) = 5.8, P -=z 0.05. The group by ear interaction was not significant. However, the planned comparison t-tests showed that the control group, as expected, had a higher right ear score compared to the left (t = 2.1, P < 0.05) while this was not so for the depressed group (f = - 1.26, P > 0.10).

TABLE

I

DICHOTIC MONITORING RESULTS FOR EACH SUBJECT GROUP ACCORDING TO EAR FOR EACH OF THE DEPENDENT VARIABLES Depressed LE

Control RE

LE

RE

HR

73

76

83

91

RT

(17) 618

(12) 605

(15) 600

(12) 562

(84) 0.92 (0.20) 0.43 (0.20)

(90) 0.91 (0.06) 0.26 (0.21)

P(A) log P

(136) 0.83 (0.09) 0.51 (0.19)

(117) 0.84 (0.06) 0.56 (0.31)

LE, left ear; RE, right ear; HR, percentage target detection; RT, reaction time (ms); P(A), target discrimination; log j3, response bias. Standard deviations are given in parentheses.

On the RT measure of the DM experiment, ANOVA revealed that the two groups did not vary significantly in the speed with which they responded to targets, but responses to right ear items (mean = 583 ms, SD = 106) were faster than to those of the left ear (mean = 609 ms, SD = 112) F(l, 45) = 4.95, P -c0.05. The group by ear interaction was not significant. Similar planned comparisons to those performed for HR showed that controls responded significantly faster to right ear targets compared to left (t = 2.1, P -c0.05) while depressed subjects showed no significant difference in RT between the ears (t = 0.93, P > 0.3). However, unlike the HR measure where the standard deviations were similar for both groups, the lack of a REA for depressed subjects on RT may have been due to comparatively greater variability in performance in depressed subjects as suggested by the standard deviation figures for RT in this group. In an attempt to determine the underlying basis for performance differences between the groups, similar ANOVAs were also carried out on the signal detection measures P(A) and /? (log-transformed scores) both of which take account of false-positive responses. Target discrimination as measured by P(A) was superior for control compared to depressed subjects, F(1, 46) = 8.26, P < 0.01, and the former group also showed a greater readiness to respond (p), F(l, 46) = 10.8, P <

5

0.01. There were no ear differences in performance on either of these measures but an interaction between group and ear was obtained for ,l?, F(1, 46) = 10.9, P < 0.01. This interaction reflected a strong response bias to the right ear compared to the left in control subjects. This was not found in the depressed group which showed a similar response bias for each ear. In schizophrenia, the syndrome comprising the BPRS items of emotional withdrawal (item 3), motor retardation (item 13) and blunted affect (item 16) can be taken as a measure of the negative symptom complex. The same constellation of symptoms observed in depressive disorders would more likely be referred to as psychomotor retardation. Having previously found an association between negative symptoms and reduced ear differences in schizophrenia (Carr and Wale, 1988), it seemed of interest to determine whether a similar reduction in ear differences would also be found in relation to the same symptom group in depression. Accordingly, the depressed subjects were divided into two subgroups depending on whether their score for ‘negative symptoms/psychomotor retardation’ (withdrawal-retardation), as measured by summation of the relevant BPRS items, fell above or below the group median. Repeated measures ANOVAs, subgroup (2) x ear (2), were then carried out on each of the dependent variables in the two tasks. Again, there were no significant main or interaction effects on the FRW measure. There were also no significant effects found for RT on the DM task. However, on HR there was a significant subgroup by ear interaction, F (1, 22) = 4.9, P < 0.05, while neither main effects (subgroup or ear) showed significant differences. The interaction effect reflected a higher left ear score and lower right ear score (i.e., no REA) for those rating high on withdrawal-retardation while those with few such symptoms showed a REA (see Table 2). Depressed subjects also showed a range of scores on an anxiety scale, a composite rating of BPRS items anxiety (item 2) and tension (item 6). There was also a negative correlation (r = - 0.64, P < 0.001) between this scale and withdrawal-retardation suggesting a low degree of overlap between these two symptom groups. A similar set of ANOVAs was performed on each dependent vari-

TABLE

2

DICHOTIC MONITORING RESULTS ACCORDING TO EAR FOR ‘HIGH’- AND ‘LOW’-SYMPTOM SUBGROUPS Subgroups High LE Withdrawal-retardation HR 76

Low RE

LE

RE

73

70

80

(16) 629

(13) 630

(18) 611

(11) 586

(176)

(133)

(103)

(105)

RT

Anxiety HR

c::,

80

76

(18) 628

65

585

(14) 610

(14) 624

(164)

(153)

(111)

(75)

RT

Standard deviations are given tions see note to Table 1.

in parentheses.

For

abbrevia-

able for the anxiety scale as had been done for withdrawal-retardation after division into highand low-scoring subgroups. Once again, no significant effects were found for the FRW data. When the DM data were analysed there were no main effects but two-way interactions were obtained on both HR, F(1, 22) = 7.5, P < 0.05, and RT, F(l, 22) = 4.97, P -C 0.05. These interactions reflected better left ear compared to right ear performances in those with low scores on this dimension, with a REA being found for those with high scores. Thus, on the HR measure in depressed subjects, high ratings for withdrawal-retardation were associated with a reversal (although small) in the normal ear asymmetry (REA). This effect on asymmetry was also found for RT as well as HR in depressed subjects with low anxiety ratings. Discussion The results suggest that attention may be an important factor in the lateral asymmetries found in association with depression. On the task of language processing with minimal attentional demands (FRW) no differences were found between depressed subjects and controls or within depressed subjects according to symptomatology. On the other hand, the task with an attentional com-

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ponent (DM) revealed differences according to both diagnosis and symptomatology. Depressed subjects detected fewer targets than controls and this was due to both poorer target discrimination and a reduced readiness to respond. However, this may have simply reflected the higher level of functioning of the control subjects rather than any specific effect of depression. The control subjects were not hospitalised or known to be suffering from any psychiatric disorder and they were not matched with the depressed subjects on any measure of intellectual function. The potential confounding effects of hospitalisation, non-specific psychopathology and intellectual functioning could not be addressed by the present study design. Contrary to intuitive expectation, the depressed group did not demonstrate slower reaction times compared to the control group, but their reaction times were more variable than those of controls. Depressed subjects also showed an absence of the normal response bias to right ear inputs; there were no significant differences between ears on the number of targets detected or on reaction times to correct items. By contrast, control subjects had a significant REA on both of these measures, although the magnitude of the ear differences did not differ significantly between the groups (i.e., no interaction effect). The failure to find a group by ear interaction on analysis of variance was undoubtedly due to the presence of a normal REA in certain depressed subjects. These individuals can evidently be identified by their symptom profile. Low levels of withdrawal-retardation in depression were associated with a normal REA for HR compared to those with high scores on this symptom dimension. Likewise, subjects with high levels of anxiety also showed a normal REA whereas this asymmetry was absent for both HR and RT in subjects with low anxiety ratings. These symptom-related differences in asymmetry were not associated with a higher overall level of performance for one subgroup over the other, but reflected slightly better left ear compared to right ear performance for the subgroups who did not show the normal REA. The DM results are consistent with those of previous researchers who have found a reduced ear asymmetry in association with unipolar de-

pression (Moscovitch et al., 1981; Johnson and Crockett, 1982) and, as in the report of Moscovitch et al. (1981) differences between depression subgroups were significant. The failure to find effects on the FRW test is consistent with Wexler’s (1986) findings on this task for psychotic subjects of mixed diagnoses and controls. This suggests that limiting measures of left hemisphere function to tasks of phonemic discrimination is inadequate for identifying the mechanisms that may contribute to differences in the performance asymmetries of depressed persons on tasks of laterality. A reduction in the level of processing for items presented to the right ear together with increased responding to left ear items could be interpreted as supporting the hypothesis of a ‘strongly primed right hemisphere’ as posited by Moscovitch et al. (1981). However, a reduction in the dominance of the left hemisphere on a verbal task and an associated decrease in interhemispheric inhibition could also explain the findings. The lack of significant effects on the primarily language discrimination task (FRW) suggests that an attentional explanation may be more satisfactory than either of the above. It is unlikely that the results are merely an effect of generalised hypoarousal. reflected more in left hemisphere attentional performance owing to the verbal nature of the task. Normal subjects with chemically induced changes in arousal have not shown this change in asymmetry on a similar DM task (Clark et al., 1987). Thus, asymmetries in attentional mechanisms appear to be important and it can be argued that hemisphere differences in attention may be interpreted to support an attentional explanation of the present results. There is evidence to suggest that the two cerebral hemispheres subserve different mechanisms of attention with the right hemisphere priniarily locating information spatially and hence attending to both sides of space while the left is more specific in identifying type of information. with spatial attention being limited to the right side (Heilman and Van Den Abell, 1979; Knight et al., 1981; Harter et al., 1982). Thus it could be postulated that any disruption of left hemisphere attentional mechanisms may produce a loss of the normal REA on dichotic tasks. Given a limited information processing system, any reduction in processing from one source (right ear) could en-

able comparatively extra capacity to be allocated to alternative sources of information (left ear). This hypothesis is also congruent with a report associating emotional factors with obtained ear asymmetries (Wexler et al., 1986). Wexler and his associates found a relationship between ‘positive’ emotional factors and increased ear differences which were postulated to reflect emotion-mediated activation of the left hemisphere via frontal attention centres. Evidence to suggest that the left hemisphere is more involved in positive emotions while negative emotions are primarily right-hemisphere-based (Dimond et al., 1976; Ahern and Schwartz, 1979) is also consistent with the formulation of Wexler and his associates. Thus the loss of REA found in association with withdrawal-retardation could be due to an absence of ‘positive’ emotion. From this viewpoint anxiety appears to be ‘positive’, at least in the context of its effects on attention and/or left hemisphere activation. Grey (1982) has suggested that anxiety in depression is associated with increased attention and arousal. An interaction between attention and affect can therefore be proposed as the basis of the performance asymmetries found in the present study. There appears to be a reciprocal relationship between anxiety and withdrawal-retardation in the depressed subjects of this study which is supported by the inverse correlation found between these two symptom dimensions. The absent REA associated with low anxiety/high withdrawal-retardation can be accounted for by a differential reduction in right ear relative to left ear performance and this implies a relative reduction in attention to dominant inputs by the left hemisphere. High anxiety/low withdrawal-retardation, on the other hand, seems to be associated with a more or less uniform reduction in both left and right ear performance levels implying a more global reduction in attentional capacity in association with this symptom profile. Such a formulation which takes into account the relationships between attention and affect can also accommodate the findings of previous studies showing a return to normal asymmetry following treatment and an alteration in affective state. It should be pointed out that the question of the relationship between attentional asymmetry and illness severity cannot be properly addressed

here. There was no overall measure of the severity of depression in this study and, therefore, it is unclear whether anxiety, withdrawal-retardation or neither of these two symptom dimensions can be taken to reflect this factor. It is noteworthy that a reduced REA has also been found on the DM task for schizophrenic subjects with prominent negative symptoms (Carr and Wale, 1988). This suggests that certain symptom variables may be associated with a common underlying process cutting across diagnostic boundaries and reflecting similar disturbances in attention and the normal balance of processing, namely relative inattention by the left hemisphere to dominant inputs. There is an accumulation of evidence from various sources (see Otto et al., 1987, for a review) implicating right hemisphere processes in depression. Otto and his associates propose that activation of the right hemisphere by aversive stimuli may be a key factor in depression and suggest that frontal inhibition may provide the modulatory control that intercedes when depressive reactions do not occur. Further, one could speculate that frontal mechanisms in the left or ‘positive’ hemisphere are crucial to this modulatory control. This is consistent with data from unilateral lesion studies showing depression to be associated more frequently with left frontal disorders (e.g., Robinson et al., 1984). The results of the present study suggest a model of depression in which the papers of Otto et al. (1987) and Robinson et al. (1984) can both be accommodated. Depressive disorder may involve, first, a right-hemisphere-centred aversive experience associated with a general decline in attentional capacity which may then be followed secondarily by either (a) a left hemisphere compensatory reaction associated with anxiety which maintains the normal pattern of perceptual asymmetry or, alternatively, (b) a failure in left frontal modulatory mechanisms resulting in a selective reduction in left hemisphere attention to dominant inputs, a process associated with the withdrawal-retardation symptom profile. The latter mechanism would result in comparatively increased attention to right hemisphere inputs, those putatively associated with the aversive or negative aspects of the depressive experience. Although these results and theoretical proposi-

8

tions are consistent with other researchers, the explanations proffered can only be regarded as tentative at this stage. Further studies are needed to clarify questions raised but not addressed in this report. The relationships between anxiety, withdrawal-retardation and overall severity of de: pression need to be investigated, as do the effects of anxiety on DM performance in non-depressed persons. Comparisons between subgroups of depressed patients and other psychiatric controls would also be more important in examining the specific functional effects of depression than comparison with normal controls where general level of functioning may be a confounding factor. The precise mechanisms involved in depression are as yet unknown but there appears to be an interaction between affect, hemisphere processes and attention. Left frontal dysfunction may underlie the performance asymmetries found in depression, particularly those related to attention. Thus anxiety and withdrawal-retardation may be the phenomenological expressions of certain underlying processes which produce differences in performance asymmetries in depression, the former being associated with a normal pattern of lateral asymmetry while the latter is associated with a left-sided dysfunction causing loss of the normal pattern of asymmetry. Acknowledgements We are grateful to Dr. G. Geffen for her help and support in the use of the dichotic monitoring task. Thanks are also due to Dr. B. Wexler and Dr. T. Halwes for permission to use the dichotic fused rhymed test. This research was supported by Grant 850266 from the National Health and Medical Research Council of Australia. References Ahern, G.L. and Schwartz, G.E. (1979) Differential localization for positive versus negative emotions. Neuropsychologia 17, 693-698. American Psychiatric Association (1980) Diagnostic and Statistical Manual of Mental Disorders, 3rd edn. APA, Washington, DC. Annett, M. (1970) A classification of hand preference by association analysis. Br. J. Psychol. 61, 303-321. Bruder, G.E. (1983) Cerebral laterality and psychopathology: a

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