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The influence of positive and negative mood states on risk taking, verbal fluency, and salivary cortisol
Journal of Affective Disorders 63 (2001) 179–187 www.elsevier.com / locate / jad
Research report
The influence of positive and negative mood states on risk taking, verbal fluency, and salivary cortisol a, b a L. Clark *, S.D. Iversen , G.M. Goodwin a
b
Department of Psychiatry, Warneford Hospital, Oxford, UK Department of Experimental Psychology, Warneford Hospital, Oxford, UK
Received 21 May 1999; received in revised form 5 October 1999; accepted 27 February 2000
Abstract Background: Neuropsychological studies in depressed and manic patients have revealed significant frontal cortex dysfunction. It is hypothesised that performance on frontal lobe tasks may be sensitive to induced fluctuations in mood state in non-clinical samples. Methods: Subjects performed one of two neuropsychological tasks immediately subsequent to a musical mood induction procedure designed to induce either elation or depression. Mood was assessed using self-report measures. Salivary cortisol levels were also measured in an attempt to objectively validate mood induction effects. The tasks used were verbal fluency and Damasio’s Gambling Game. Two groups of subjects were recruited: a group with previous (subclinical) hypomanic experience (n 5 23) and a control group without previous hypomanic experience (n 5 23). Results: The positive and negative mood inductions produced robust and contrasting effects on self-reported mood, but had no significant differential effects on salivary cortisol levels and neuropsychological performance. Limitations: The findings are restricted by the absence of a neutral mood control condition. Conclusions: Salivary cortisol recording does not provide a simple and reliable method of validating psychological mood induction. Performance on frontal lobe tests appears to be insensitive to normal mood fluctuations, which supports the argument that the deficits in mood disorder patient groups may instead reflect core disturbances of neurobiological processes. 2001 Elsevier Science B.V. All rights reserved. Keywords: Hypomania; Mood induction; Prefrontal; Risk taking; Fluency; Salivary cortisol
1. Introduction Affective disorders have traditionally been investigated using two approaches: studies in patient samples, and studies of normal volunteers who have had *Corresponding author. University Department of Psychiatry, Neurosciences Building, Warneford Hospital, Oxford OX3 7JX, UK. Tel.: 1 44-1865-226-492; fax: 1 44-1865-251-076.
mood states induced through either a psychological or pharmacological procedure. It has been argued that transient, induced negative mood in normals may be analogous to mild, naturally occurring depression (Clark, 1983). In contrast, the relationship between mania or hypomania, and induced positive mood in normals is virtually unexplored. This is a little surprising considering the inherent practical difficulties of testing acutely manic patients, as well
0165-0327 / 01 / $ – see front matter 2001 Elsevier Science B.V. All rights reserved. PII: S0165-0327( 00 )00183-X
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as the potentially confounding effects of their medication. Two of the most prominent clinical symptoms of mania are pressure of speech, and poor decisionmaking. We decided to employ neuropsychological tests likely to reflect performance in these domains of cognitive function. For pressure of speech, we planned to use tests of verbal fluency, which are sensitive to frontal lobe dysfunction; particularly in left dorsolateral prefrontal cortex (left dlPFC) (Borkowski et al., 1967; Frith et al., 1991). Abnormal activation of left dlPFC has been implicated in clinical depression (Bench et al., 1992) and induced happy and sad mood states in normals (Gemar et al., 1996; Baker et al., 1997). The decision-making abnormality characteristic of mania is a tendency to make impulsive decisions associated with high risk of punishment, especially involving money and social or sexual liaisons. Patients with focal brain damage to ventral prefrontal cortex (vPFC) often show a disinhibition syndrome which is reminiscent of manic behaviour (cf. Damasio, 1994). Furthermore, there is evidence that vPFC is abnormally activated in mood disorder patients (Drevets et al., 1997; Goodwin et al., 1997), and is also involved in normal mood changes (Baker et al., 1997). The decision-making impairment displayed in vPFC patients can be isolated with a task known as the Gambling Game (Bechara et al., 1994), which will be described in detail below. Unlike normal subjects, vPFC patients persist in making risky choices, driven by immediate reward and despite long-term punishment. It is hypothesised that manic mood will reveal the same pattern of impairment, possibly also due to vPFC dysfunction. We hypothesised that induced positive mood would be associated with higher production on verbal fluency and more risky choices on the gambling game. To maximise the effectiveness of the positive mood induction, a group of subjects were recruited with previous experience of subclinical hypomanic symptoms, in the expectation that they would show higher susceptibility to a positive mood induction. Mood induction procedures are sometimes criticised because they rely so heavily on subjective reports of mood change. In particular, there is the
issue of demand characteristics; subjects report mood changes simply to comply with the demands of the experiment (Polivy and Doyle, 1980; Buchwald et al., 1981). However, Brown et al. (1993) reported that both positive and negative mood inductions produce increases in serum cortisol levels for approximately 1 h after the induction procedure. Detection of this effect in salivary cortisol samples might provide a simple means of validating the self-report ratings with an independent measure of physiology.
2. Method
2.1. Subjects Ethical approval for the experiment was obtained from the local ethics committee. Subjects were identified using a screening questionnaire adapted from DSM-IV diagnostic criteria for a hypomanic episode (American Psychiatric Association, 1994). The questionnaire enquired whether subjects had ever experienced an episode resembling hypomania, but required milder symptomatology than DSM-IV criteria: only 3 or more days of elated or extremely good mood, accompanied by at least two of 10 further symptoms; specifically, increased talkativeness, decreased need for sleep, racing thoughts, irritability, excessive spending, increased productivity, excessive optimism, restlessness, distractability, and grandiose ideas. Twenty-three subjects had experienced episodes meeting these criteria in the past and thus represented a ‘hypomanic’ group; 23 subjects replied to the questionnaire but claimed to have not experienced such episodes in the past and thus represented a control group.
2.2. Personality measures Subjects completed the following personality measures: (1) Eysenck Personality Questionnaire (Short Version) (Eysenck and Eysenck, 1975); (2) ManicDepressiveness Scale (Thalbourne et al., 1994); (3) Social Desirability Scale (Crowne and Marlowe, 1964); (4) Affect Intensity Measure (Larsen and Diener, 1985); and (5) State-Trait Anxiety Inventory (Spielberger et al., 1983). Subjects were also ad-
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ministered the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I; First et al., 1997).
2.3. Procedure Subjects engaged in two psychological mood induction procedures: one positive, one negative. The musical mood induction procedure described by Clark and Teasdale (1985) was used in the experiment. The negative piece of music was Prokofiev’s Russia Under the Mongolian Yoke, slowed to halfspeed. The positive piece of music was Delibes’ Coppelia. These pieces have been validated in several previous mood induction studies (see Gerrards-Hesse et al., 1994, for review). Subjects listened to the music through headphones, and were left undisturbed for the duration of the music (approx. 5 min). After each mood induction procedure, subjects performed one of two neuropsychological tasks, in a within-subjects crossover design. The first neuropsychological task was a computerised version of the Gambling Game (Bechara et al., 1994). In this task, subjects are presented with four decks of cards, and must make a long series of card selections. On all card choices subjects win money, but on some choices subjects also lose money. Decks A and B are characterised by high wins ($100 per choice), but higher losses, such that there is net loss of money. Decks C and D have lower wins (only $50) but milder losses such that there is a net gain. Subjects must deduce these contingencies in order to fulfil the instruction to win as much money as they can. The second task was verbal fluency using the letters F, A, and S (Borkowski et al., 1967), and semantic fluency (animals and furniture). With the verbal fluency task, subjects also performed paced and fast counting from 1 to 10 (Teasdale et al., 1980). Each of the neuropsychological tests took around 8–10 min to complete. Mood was assessed using Visual Analogue Scales (Bond and Lader, 1974) for depression, elation, anxiety, and boredom, and the Befindlichskeits-skala (BFS; von Zerssen et al., 1974), a checklist consisting of 28 pairs of adjectives relating to current mood. These two methods of mood assessment were both
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given at four points during each mood induction procedure: at time 0 (baseline); at time 10 min immediately after the mood induction; at time 15, a midpoint during the neuropsychological task; and at time 20 after completion. Salivary cortisol samples were also obtained at these time points using salivette tubes (Sarstedt): cotton-wool sticks which were placed in the mouth during completion of the mood ratings. Due to diurnal variation in cortisol levels, all testing was conducted between 13:00 and 16:00 h. Salivary cortisol was measured by radioimmunoassay (Franklin et al., 1998). The mean inter-assay coefficient of variation was , 10% and the sensitivity was 0.1 mg / ml. Between the two mood induction procedures, all subjects watched a 25-min gardening television programme, to minimise any carry-over of mood from the first mood induction to the second. Subjects were encouraged to be fully honest in their mood ratings, and also completed a post-experiment mood check, asking whether they experienced a genuine mood shift in each mood induction period.
3. Results
3.1. Group characteristics Forty-six subjects were recruited; 23 in each group. Five subjects (two controls, three hypomanics) responded negatively to the post-experiment mood check and were therefore excluded from all analysis. Demographic characteristics of the two groups are presented in Table 1. There were no significant differences in age or NART IQ score between the two groups. Of the hypomanic subjects, 11 met DSM-IV criteria for Bipolar-II Disorder, and a further one subject met criteria for a major depressive episode, assessed using the SCID diagnostic manual. Of the control subjects, four met criteria for a previous major depressive episode; none had experienced hypomania. Significant differences on personality measures between hypomanic subjects and controls were revealed on two scales: the Manic-Depressiveness Scale and the Affect Intensity Measure (see Table 1). Scores on these two scales were themselves highly correlated (Pearson’s r 5 0.61, P , 0.001).
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Table 1 Group characteristics, and personality measures for hypomanic and control subjects: mean (S.E.M.)
Male:female ratio Mean age Mean NART errors
Control subjects (n 5 21)
Hypomanic subjects (n 5 20)
11:10 21.4 (0.41) 14.1 (1.4)
8:12 21.2 (0.58) 16.7 (1.1)
EPQ a -Extraversion EPQ-Neuroticism EPQ-Psychoticism EPQ-Lie scale
7.83 (0.78) 5.78 (0.91) 3.44 (0.54) 3.00 (0.50)
9.25 6.65 3.80 2.80
MDS a -Depression MDS-Mania MDS-Total
2.72 (0.47) 4.00 (0.40) 6.72 (0.64)
3.95 (0.47) 5.80 (0.30)** 9.75 (0.55)**
Social desirability scale State anxiety score Trait anxiety score Affect intensity measure
13.0 33.4 38.8 130.9
(1.2) (2.6) (2.4) (5.4)
12.2 36.1 42.5 158.4
(0.63) (0.72) (0.42) (0.49)
(0.96) (2.5) (2.0) (4.2)***
a EPQ, Eysenck Personality Questionnaire; MDS, Manic Depressiveness Scale. **P , 0.005; ***P , 0.0005. Independent samples t-test.
3.2. Effects of mood induction procedures on subjective mood ratings Two-way repeated-measures ANOVAs of mood condition (positive, negative) by time (four-level) revealed a significant interaction on VAS Depression (F(3,120) 5 37.35, P , 0.001), VAS Elation (F(3,120) 5 58.81, P , 0.001), VAS Anxiety (F(3,72) 5 8.73, P , 0.001), VAS Boredom (F(3,120) 5 9.96, P , 0.001) and the BFS (F(3,120) 5 49.14, P , 0.001). When group (hypomanics, controls) and history of depression were considered as between-subjects variables in these analyses, the three-way interaction terms were not significant in any cases. Thus mood induction was associated with the expected changes in subjective ratings but without evidence of a greater sensitivity in the hypomanic subjects (see Fig. 1, Table 2).
3.3. Effects of mood induction procedures on salivary cortisol Twenty-two subjects had complete salivary cortisol data for the positive mood induction (10 hypomanics, 12 controls). Repeated-measures
Fig. 1. Change from baseline on Visual Analogue Scales for Elation (6S.E.M.) during positive and negative mood induction procedures, for hypomanic and control subjects. Musical mood inductions ran from approximately 3 to 10 min. One-way ANOVA revealed no differences between four groups at baseline (F(3,78) 5 0.169, P 5 0.917). Open squares, hypomanics, positive mood induction; open circles, hypomanics, negative mood induction; closed squares, controls, positive mood induction; closed circles, controls, negative mood induction.
ANOVA did not reveal a main effect of time (P 5 0.161). When group, gender, and history of depression were considered as between-subjects variables, no interaction terms reached significance. Twenty-six subjects had complete salivary cortisol data for the negative mood induction (11 hypomanics, 15 controls). Repeated-measures ANOVA revealed a significant main effect of time on salivary cortisol level across the sample as a whole (F(3,75) 5 4.98, P , 0.005), such that cortisol levels tended to drop over the 20 min of the mood induction. There were no interactions between salivary cortisol levels and group (hypomanics, controls), gender, or history of depression.
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Table 2 Subjective mood ratings during positive and negative mood inductions: mean (S.E.M.)
VAS depression (mm) VAS elation (mm) VAS anxiety (mm) VAS boredom (mm) BFS total
Positive*** Negative*** Positive*** Negative*** Positive*** Negative** Positive*** Negative Positive*** Negative***
Baseline T0
Time 10
Time 15
Time 20
31.9 31.4 49.6 51.0 33.7 27.3 42.8 38.7 13.2 12.5
17.1 (2.0) 51.0 (2.7) 68.5 (1.8) 33.6 (2.1) 20.5 (3.2) 40.9 (4.7) 23.6 (2.6) 37.5 (2.8) 6.7 (0.99) 26.5 (1.7)
22.7 49.3 64.8 32.3 24.7 40.6 25.5 36.6 8.8 27.6
26.0 40.6 64.1 44.7 24.0 31.4 25.5 35.0 8.2 19.2
(2.9) (2.9) (2.6) (2.2) (4.1) (4.0) (3.1) (3.3) (1.6) (1.4)
(2.5) (3.0) (2.4) (2.3) (3.5) (4.7) (3.1) (2.7) (1.1) (2.1)
(2.8) (3.0) (2.2) (2.0) (3.9) (3.7) (3.1) (3.1) (1.0) (2.1)
**P , 0.005; ***P , 0.0005. Repeated-measures ANOVA with time as a four-level single factor. When group (hypomanic, control) and history of depression were considered as between-subjects variables in these analyses, no interaction terms reached significance.
A two-way repeated-measured ANOVA was calculated for mood condition (positive, negative) 3 time (four-level). There was a significant main effect of time (F(3,57) 5 3.91, P 5 0.013), but no main effect of mood induction condition (P 5 0.239). The interaction between mood induction condition and time was also non-significant (P 5 0.161). When group, gender, and history of depression, were considered as between-subjects variables in this analysis, no interaction terms reached significance. Thus mood induction was associated with a salivary cortisol profile which did not differ between mood condition, did not differ between hypomanic and control subjects, and showed no clear-cut elevation from baseline (see Fig. 2). It is possible that mood induction may have attenuated the normal drop in salivary cortisol levels that occurs when subjects are at rest (e.g., Brown et al., 1993). This was examined by comparing the drop in salivary cortisol during the mood induction procedures (time 0 minus time 20) to the drop during the neutral gardening programme, which lasted roughly the same time. The drop in salivary cortisol level during the positive mood induction and the neutral video did differ but not significantly (positive mood, change from baseline, mean 5 2 1.19, S.E.M. 5 0.734; neutral, mean 5 2 2.73, S.E.M. 5 0.890; P 5 0.095). There was no difference in the drop in salivary cortisol between the negative mood induction and the neutral video (negative mood, change from baseline, mean 5 2 2.85, S.E.M. 5 0.687; neutral, mean 5 2 2.73, S.E.M. 5 0.890; P 5 0.918). The drop in salivary cortisol during the
Fig. 2. Change from baseline in salivary cortisol level (6S.E.M.) during positive and negative mood induction procedures, for hypomanic and control subjects. Musical mood inductions ran from approximately 3 to 10 min. One-way ANOVA reveals no differences between four groups at baseline (F(3,44) 5 1.078, P 5 0.37). Open squares, hypomanics, positive mood induction; open circles, hypomanics, negative mood induction; closed squares, controls, positive mood induction; closed circles, controls, negative mood induction.
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positive and negative conditions did differ, but again, the difference was not significant (P 5 0.074). When group, gender, and past depression were considered as between-subjects variables in these analyses, none were found to be significant. Hence mood induction was not found to attenuate the normal drop in salivary cortisol during rest.
3.4. Effects of mood induction procedure on neuropsychological performance One-way ANOVAs testing the effects of mood condition on performance revealed no significant effects of mood on gambling game performance (total number of risky choices) (P 5 0.809), category fluency (P 5 0.921), paced counting (P 5 0.705), and fast counting (P 5 0.509) (see Table 3). There was a significant effect of mood on letter fluency (F(1,39) 5 4.80, P 5 0.035) such that subjects in the negative mood condition produced higher verbal output in 3 min relative to subjects in the positive mood condition. When group (hypomanics, controls) and history of depression were considered as second between-subjects variables in these analyses, there were no significant main effects or interaction terms on any of the neuropsychological variables.
3.5. Associations between personality variables, neuropsychological and neuroendocrine measures A significant correlation was found between number of risky choices on the Gambling game and score on the Manic Depressiveness Scale (Pearson’s r 5 0.35, P 5 0.029), such that individuals with more prior manic-depressive experiences tended to make
more risky choices. The depression subscale of the MDS correlated with gambling performance (r 5 0.40, P 5 0.012) but the mania subscale did not. No other personality variables correlated with neuropsychological performance. Associations between personality variables and salivary cortisol response were examined using summed changes from baseline (at times 10, 15, 20) as a single figure of cortisol response. There were no significant correlations between personality variables and salivary cortisol response during either positive or negative mood inductions.
4. Discussion The aim of the present study was to demonstrate differential effects of induced positive and negative moods in a non-clinical sample on two neuropsychological tests: verbal fluency and the gambling game. Salivary cortisol measures were recorded in an effort to validate the efficacy of the mood inductions. Self-report data from the visual analogue scales and the BFS indicate the positive mood induction achieved a robust effect of elation lasting for the duration of the procedure, whilst the negative mood induction achieved a robust and lasting effect of depression. These contrasting mood states, however, were without major effects at the neuroendocrine and neuropsychological levels. There were no significant differences between salivary cortisol levels during the positive and negative mood inductions. The drop in cortisol levels during the two mood inductions did not significantly differ from the drop in cortisol level whilst subjects
Table 3 Verbal fluency and gambling game performance for hypomanic and control subjects after positive and negative mood induction procedures (MIPs) Hypomanics
Fluency, FAS Fluency, category Paced counting (s) Fast counting (s) Gambling game: risky (AB) choices (%)
Controls
Positive MIP (n 5 10)
Negative MIP (n 5 10)
Positive MIP (n 5 11)
Negative MIP (n 5 10)
41.2 (3.4) 42.5 (3.2) 5.99 (0.68) 1.32 (0.12) 42.3 (3.6)
53.9 (3.9) 40.9 (2.9) 5.85 (0.97) 1.35 (0.09) 40.6 (4.5)
45.9 (4.6) 41.7 (2.4) 5.58 (0.94) 1.22 (0.10) 43.2 (2.1)
49.8 (2.8) 43.8 (1.6) 6.32 (0.61) 1.31 (0.04) 43.1 (3.7)
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watched a gardening video, which is suggested to serve as a neutral mood control condition. These data fail to support the results of Brown et al. (1993) who found a gradual rise in serum cortisol levels in the 60 min subsequent to both positive and negative mood inductions. There is no reason to suppose that fluctuations in serum cortisol levels cannot be detected as easily in salivary samples as in plasma. It is conceivable that the effect on salivary cortisol may not be detectable within the first 10 min subsequent to the mood induction. However, if it were a delayed effect, we would have expected to see it during the subsequent neutral video condition, which was not the case. Alternatively, it may be significant that Brown et al. recorded resting cortisol levels for 135 min prior to the mood induction procedure, allowing the cortisol level to reach its nadir. Whatever the explanation, the results of this study do not support salivary cortisol measurement as a simple and reliable objective method of validating psychological mood induction. It was hypothesised that positive mood would be associated with increased risky decision-making on the Gambling Game, which may be indicative of vPFC involvement in normal and pathological mood processes. The hypothesis was not supported; there were no differences in gambling game performance between positive and negative mood conditions. In the absence of a neutral mood control condition, it is feasible that positive and negative mood both influence decision-making in a similar manner. This is considered unlikely for two reasons. Firstly, our data closely resemble the control data from 44 subjects from the Bechara et al. (1994) original report. Secondly, there is evidence that depressed mood is associated with reduced sensitivity to reward (e.g., Costello, 1972; Henriques et al., 1994); hence depressed subjects should derive less benefit from risky choices, and so we would predict positive and negative induced moods to have opposing effects on gambling game performance. Verbal fluency performance was also examined in relation to positive and negative induced mood, with the hypothesis that positive mood would be associated with higher verbal output that negative mood (Table 3). There were no differences in category fluency performance between mood conditions, and on FAS fluency the opposite effect was found:
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negative mood was associated with higher verbal fluency than positive mood. In the absence of a neutral mood control condition it is impossible to ascertain whether this effect is specific to negative mood or positive mood, or whether the two states have opposing, and counterintuitive, effects on verbal fluency. There are a number of reports indicating verbal fluency is reduced in clinical depression and that it is state dependent (e.g., Trichard et al., 1995), so this finding with mood induction must await replication. In an attempt to maximise the effectiveness of the positive mood induction, a group of subjects with previous subclinical hypomanic experience were recruited. This is a novel approach in research into mania. Subjects with previous hypomanic experience and control subjects showed similar mood shifts on the self-report scales, similar salivary cortisol effects, and performed similarly on the neuropsychological tasks. The hypothesis that the subjects with previous hypomanic experience would show higher susceptibility to positive mood induction was thus refuted. A correlation was revealed between score on the Manic-Depressiveness Scale and risky choices on the gambling game, however. This may represent a trait marker in the hypomanic subjects, associated with riskiness or impulsivity. It does not appear to be influenced by state fluctuations in normal mood. The two subject groups were both recruited using a screening questionnaire adapted from DSM-IV criteria for a hypomanic episode. However, the criteria on the questionnaire required a milder episode than DSM-IV criteria, and there are no previous studies in the literature validating this questionnaire. Eleven subjects in the group with hypomanic experience met formal criteria for Bipolar II Disorder when assessed with the SCID (First et al., 1997), and the group scored significantly higher than controls on the Manic-Depressiveness Scale (Thalbourne et al., 1994), a measure of previous bipolar experiences; and the AIM (Larsen and Diener, 1985), a measure of the tendency to experience extreme rather than mild forms of emotion. These findings lend support to the argument that this group may represent the mild end of the bipolar spectrum. However, none of the subjects in this group had consulted a psychiatrist about their mood, or had received any psychiatric treatment. They must therefore be considered a non-
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clinical sample, and as such, the generalisability of these findings to a clinical sample of bipolar patients is unclear. The authors are unaware of any published studies investigating positive mood induction in bipolar patients, but the present results raise the possibility that bipolar patients would not show an increased susceptibility to positive mood induction and would not manifest a neuropsychological ‘relapse’ under conditions of mood induction. The present findings are critical to the interpretation of neuropsychological studies in pathological mood states. Major depression and mania have both been associated with deficits on neuropsychological tasks sensitive to prefrontal cortex dysfunction (Morice, 1990; Dolan et al., 1994; Beats et al., 1996). It is possible, however, that these impairments are merely a temporary feature of affective disturbance, and prefrontal task performance may be influenced by relatively subtle changes in mood. The present findings, although in a non-clinical sample, indicate this is unlikely. They give weight to the argument that the reported deficits in mood disorder patients are associated with a stable, state-related abnormality in prefrontal cortex and, moreover, that neuropsychological assessments in mood disorder patients provide insight into the underlying neural mechanisms of mood disorder.
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Trichard, C., Martinot, J.L., Alagille, M., Masure, M.C., Hardy, P., Ginestet, D., Feline, A., 1995. Time course of prefrontal lobe dysfunction in severely depressed in-patients: a longitudinal neuropsychological study. Psychol. Med. 25, 79–85. von Zerssen, D., Strian, F., Schwarz, D., 1974. Evaluation of depressive states, especially in longitudinal studies. In: Pichot, P. (Ed.), Psychological Measurements in Psychopharmacology. Karger, Basel, Switzerland, pp. 189–202.
Research report
The influence of positive and negative mood states on risk taking, verbal fluency, and salivary cortisol a, b a L. Clark *, S.D. Iversen , G.M. Goodwin a
b
Department of Psychiatry, Warneford Hospital, Oxford, UK Department of Experimental Psychology, Warneford Hospital, Oxford, UK
Received 21 May 1999; received in revised form 5 October 1999; accepted 27 February 2000
Abstract Background: Neuropsychological studies in depressed and manic patients have revealed significant frontal cortex dysfunction. It is hypothesised that performance on frontal lobe tasks may be sensitive to induced fluctuations in mood state in non-clinical samples. Methods: Subjects performed one of two neuropsychological tasks immediately subsequent to a musical mood induction procedure designed to induce either elation or depression. Mood was assessed using self-report measures. Salivary cortisol levels were also measured in an attempt to objectively validate mood induction effects. The tasks used were verbal fluency and Damasio’s Gambling Game. Two groups of subjects were recruited: a group with previous (subclinical) hypomanic experience (n 5 23) and a control group without previous hypomanic experience (n 5 23). Results: The positive and negative mood inductions produced robust and contrasting effects on self-reported mood, but had no significant differential effects on salivary cortisol levels and neuropsychological performance. Limitations: The findings are restricted by the absence of a neutral mood control condition. Conclusions: Salivary cortisol recording does not provide a simple and reliable method of validating psychological mood induction. Performance on frontal lobe tests appears to be insensitive to normal mood fluctuations, which supports the argument that the deficits in mood disorder patient groups may instead reflect core disturbances of neurobiological processes. 2001 Elsevier Science B.V. All rights reserved. Keywords: Hypomania; Mood induction; Prefrontal; Risk taking; Fluency; Salivary cortisol
1. Introduction Affective disorders have traditionally been investigated using two approaches: studies in patient samples, and studies of normal volunteers who have had *Corresponding author. University Department of Psychiatry, Neurosciences Building, Warneford Hospital, Oxford OX3 7JX, UK. Tel.: 1 44-1865-226-492; fax: 1 44-1865-251-076.
mood states induced through either a psychological or pharmacological procedure. It has been argued that transient, induced negative mood in normals may be analogous to mild, naturally occurring depression (Clark, 1983). In contrast, the relationship between mania or hypomania, and induced positive mood in normals is virtually unexplored. This is a little surprising considering the inherent practical difficulties of testing acutely manic patients, as well
0165-0327 / 01 / $ – see front matter 2001 Elsevier Science B.V. All rights reserved. PII: S0165-0327( 00 )00183-X
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as the potentially confounding effects of their medication. Two of the most prominent clinical symptoms of mania are pressure of speech, and poor decisionmaking. We decided to employ neuropsychological tests likely to reflect performance in these domains of cognitive function. For pressure of speech, we planned to use tests of verbal fluency, which are sensitive to frontal lobe dysfunction; particularly in left dorsolateral prefrontal cortex (left dlPFC) (Borkowski et al., 1967; Frith et al., 1991). Abnormal activation of left dlPFC has been implicated in clinical depression (Bench et al., 1992) and induced happy and sad mood states in normals (Gemar et al., 1996; Baker et al., 1997). The decision-making abnormality characteristic of mania is a tendency to make impulsive decisions associated with high risk of punishment, especially involving money and social or sexual liaisons. Patients with focal brain damage to ventral prefrontal cortex (vPFC) often show a disinhibition syndrome which is reminiscent of manic behaviour (cf. Damasio, 1994). Furthermore, there is evidence that vPFC is abnormally activated in mood disorder patients (Drevets et al., 1997; Goodwin et al., 1997), and is also involved in normal mood changes (Baker et al., 1997). The decision-making impairment displayed in vPFC patients can be isolated with a task known as the Gambling Game (Bechara et al., 1994), which will be described in detail below. Unlike normal subjects, vPFC patients persist in making risky choices, driven by immediate reward and despite long-term punishment. It is hypothesised that manic mood will reveal the same pattern of impairment, possibly also due to vPFC dysfunction. We hypothesised that induced positive mood would be associated with higher production on verbal fluency and more risky choices on the gambling game. To maximise the effectiveness of the positive mood induction, a group of subjects were recruited with previous experience of subclinical hypomanic symptoms, in the expectation that they would show higher susceptibility to a positive mood induction. Mood induction procedures are sometimes criticised because they rely so heavily on subjective reports of mood change. In particular, there is the
issue of demand characteristics; subjects report mood changes simply to comply with the demands of the experiment (Polivy and Doyle, 1980; Buchwald et al., 1981). However, Brown et al. (1993) reported that both positive and negative mood inductions produce increases in serum cortisol levels for approximately 1 h after the induction procedure. Detection of this effect in salivary cortisol samples might provide a simple means of validating the self-report ratings with an independent measure of physiology.
2. Method
2.1. Subjects Ethical approval for the experiment was obtained from the local ethics committee. Subjects were identified using a screening questionnaire adapted from DSM-IV diagnostic criteria for a hypomanic episode (American Psychiatric Association, 1994). The questionnaire enquired whether subjects had ever experienced an episode resembling hypomania, but required milder symptomatology than DSM-IV criteria: only 3 or more days of elated or extremely good mood, accompanied by at least two of 10 further symptoms; specifically, increased talkativeness, decreased need for sleep, racing thoughts, irritability, excessive spending, increased productivity, excessive optimism, restlessness, distractability, and grandiose ideas. Twenty-three subjects had experienced episodes meeting these criteria in the past and thus represented a ‘hypomanic’ group; 23 subjects replied to the questionnaire but claimed to have not experienced such episodes in the past and thus represented a control group.
2.2. Personality measures Subjects completed the following personality measures: (1) Eysenck Personality Questionnaire (Short Version) (Eysenck and Eysenck, 1975); (2) ManicDepressiveness Scale (Thalbourne et al., 1994); (3) Social Desirability Scale (Crowne and Marlowe, 1964); (4) Affect Intensity Measure (Larsen and Diener, 1985); and (5) State-Trait Anxiety Inventory (Spielberger et al., 1983). Subjects were also ad-
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ministered the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I; First et al., 1997).
2.3. Procedure Subjects engaged in two psychological mood induction procedures: one positive, one negative. The musical mood induction procedure described by Clark and Teasdale (1985) was used in the experiment. The negative piece of music was Prokofiev’s Russia Under the Mongolian Yoke, slowed to halfspeed. The positive piece of music was Delibes’ Coppelia. These pieces have been validated in several previous mood induction studies (see Gerrards-Hesse et al., 1994, for review). Subjects listened to the music through headphones, and were left undisturbed for the duration of the music (approx. 5 min). After each mood induction procedure, subjects performed one of two neuropsychological tasks, in a within-subjects crossover design. The first neuropsychological task was a computerised version of the Gambling Game (Bechara et al., 1994). In this task, subjects are presented with four decks of cards, and must make a long series of card selections. On all card choices subjects win money, but on some choices subjects also lose money. Decks A and B are characterised by high wins ($100 per choice), but higher losses, such that there is net loss of money. Decks C and D have lower wins (only $50) but milder losses such that there is a net gain. Subjects must deduce these contingencies in order to fulfil the instruction to win as much money as they can. The second task was verbal fluency using the letters F, A, and S (Borkowski et al., 1967), and semantic fluency (animals and furniture). With the verbal fluency task, subjects also performed paced and fast counting from 1 to 10 (Teasdale et al., 1980). Each of the neuropsychological tests took around 8–10 min to complete. Mood was assessed using Visual Analogue Scales (Bond and Lader, 1974) for depression, elation, anxiety, and boredom, and the Befindlichskeits-skala (BFS; von Zerssen et al., 1974), a checklist consisting of 28 pairs of adjectives relating to current mood. These two methods of mood assessment were both
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given at four points during each mood induction procedure: at time 0 (baseline); at time 10 min immediately after the mood induction; at time 15, a midpoint during the neuropsychological task; and at time 20 after completion. Salivary cortisol samples were also obtained at these time points using salivette tubes (Sarstedt): cotton-wool sticks which were placed in the mouth during completion of the mood ratings. Due to diurnal variation in cortisol levels, all testing was conducted between 13:00 and 16:00 h. Salivary cortisol was measured by radioimmunoassay (Franklin et al., 1998). The mean inter-assay coefficient of variation was , 10% and the sensitivity was 0.1 mg / ml. Between the two mood induction procedures, all subjects watched a 25-min gardening television programme, to minimise any carry-over of mood from the first mood induction to the second. Subjects were encouraged to be fully honest in their mood ratings, and also completed a post-experiment mood check, asking whether they experienced a genuine mood shift in each mood induction period.
3. Results
3.1. Group characteristics Forty-six subjects were recruited; 23 in each group. Five subjects (two controls, three hypomanics) responded negatively to the post-experiment mood check and were therefore excluded from all analysis. Demographic characteristics of the two groups are presented in Table 1. There were no significant differences in age or NART IQ score between the two groups. Of the hypomanic subjects, 11 met DSM-IV criteria for Bipolar-II Disorder, and a further one subject met criteria for a major depressive episode, assessed using the SCID diagnostic manual. Of the control subjects, four met criteria for a previous major depressive episode; none had experienced hypomania. Significant differences on personality measures between hypomanic subjects and controls were revealed on two scales: the Manic-Depressiveness Scale and the Affect Intensity Measure (see Table 1). Scores on these two scales were themselves highly correlated (Pearson’s r 5 0.61, P , 0.001).
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Table 1 Group characteristics, and personality measures for hypomanic and control subjects: mean (S.E.M.)
Male:female ratio Mean age Mean NART errors
Control subjects (n 5 21)
Hypomanic subjects (n 5 20)
11:10 21.4 (0.41) 14.1 (1.4)
8:12 21.2 (0.58) 16.7 (1.1)
EPQ a -Extraversion EPQ-Neuroticism EPQ-Psychoticism EPQ-Lie scale
7.83 (0.78) 5.78 (0.91) 3.44 (0.54) 3.00 (0.50)
9.25 6.65 3.80 2.80
MDS a -Depression MDS-Mania MDS-Total
2.72 (0.47) 4.00 (0.40) 6.72 (0.64)
3.95 (0.47) 5.80 (0.30)** 9.75 (0.55)**
Social desirability scale State anxiety score Trait anxiety score Affect intensity measure
13.0 33.4 38.8 130.9
(1.2) (2.6) (2.4) (5.4)
12.2 36.1 42.5 158.4
(0.63) (0.72) (0.42) (0.49)
(0.96) (2.5) (2.0) (4.2)***
a EPQ, Eysenck Personality Questionnaire; MDS, Manic Depressiveness Scale. **P , 0.005; ***P , 0.0005. Independent samples t-test.
3.2. Effects of mood induction procedures on subjective mood ratings Two-way repeated-measures ANOVAs of mood condition (positive, negative) by time (four-level) revealed a significant interaction on VAS Depression (F(3,120) 5 37.35, P , 0.001), VAS Elation (F(3,120) 5 58.81, P , 0.001), VAS Anxiety (F(3,72) 5 8.73, P , 0.001), VAS Boredom (F(3,120) 5 9.96, P , 0.001) and the BFS (F(3,120) 5 49.14, P , 0.001). When group (hypomanics, controls) and history of depression were considered as between-subjects variables in these analyses, the three-way interaction terms were not significant in any cases. Thus mood induction was associated with the expected changes in subjective ratings but without evidence of a greater sensitivity in the hypomanic subjects (see Fig. 1, Table 2).
3.3. Effects of mood induction procedures on salivary cortisol Twenty-two subjects had complete salivary cortisol data for the positive mood induction (10 hypomanics, 12 controls). Repeated-measures
Fig. 1. Change from baseline on Visual Analogue Scales for Elation (6S.E.M.) during positive and negative mood induction procedures, for hypomanic and control subjects. Musical mood inductions ran from approximately 3 to 10 min. One-way ANOVA revealed no differences between four groups at baseline (F(3,78) 5 0.169, P 5 0.917). Open squares, hypomanics, positive mood induction; open circles, hypomanics, negative mood induction; closed squares, controls, positive mood induction; closed circles, controls, negative mood induction.
ANOVA did not reveal a main effect of time (P 5 0.161). When group, gender, and history of depression were considered as between-subjects variables, no interaction terms reached significance. Twenty-six subjects had complete salivary cortisol data for the negative mood induction (11 hypomanics, 15 controls). Repeated-measures ANOVA revealed a significant main effect of time on salivary cortisol level across the sample as a whole (F(3,75) 5 4.98, P , 0.005), such that cortisol levels tended to drop over the 20 min of the mood induction. There were no interactions between salivary cortisol levels and group (hypomanics, controls), gender, or history of depression.
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Table 2 Subjective mood ratings during positive and negative mood inductions: mean (S.E.M.)
VAS depression (mm) VAS elation (mm) VAS anxiety (mm) VAS boredom (mm) BFS total
Positive*** Negative*** Positive*** Negative*** Positive*** Negative** Positive*** Negative Positive*** Negative***
Baseline T0
Time 10
Time 15
Time 20
31.9 31.4 49.6 51.0 33.7 27.3 42.8 38.7 13.2 12.5
17.1 (2.0) 51.0 (2.7) 68.5 (1.8) 33.6 (2.1) 20.5 (3.2) 40.9 (4.7) 23.6 (2.6) 37.5 (2.8) 6.7 (0.99) 26.5 (1.7)
22.7 49.3 64.8 32.3 24.7 40.6 25.5 36.6 8.8 27.6
26.0 40.6 64.1 44.7 24.0 31.4 25.5 35.0 8.2 19.2
(2.9) (2.9) (2.6) (2.2) (4.1) (4.0) (3.1) (3.3) (1.6) (1.4)
(2.5) (3.0) (2.4) (2.3) (3.5) (4.7) (3.1) (2.7) (1.1) (2.1)
(2.8) (3.0) (2.2) (2.0) (3.9) (3.7) (3.1) (3.1) (1.0) (2.1)
**P , 0.005; ***P , 0.0005. Repeated-measures ANOVA with time as a four-level single factor. When group (hypomanic, control) and history of depression were considered as between-subjects variables in these analyses, no interaction terms reached significance.
A two-way repeated-measured ANOVA was calculated for mood condition (positive, negative) 3 time (four-level). There was a significant main effect of time (F(3,57) 5 3.91, P 5 0.013), but no main effect of mood induction condition (P 5 0.239). The interaction between mood induction condition and time was also non-significant (P 5 0.161). When group, gender, and history of depression, were considered as between-subjects variables in this analysis, no interaction terms reached significance. Thus mood induction was associated with a salivary cortisol profile which did not differ between mood condition, did not differ between hypomanic and control subjects, and showed no clear-cut elevation from baseline (see Fig. 2). It is possible that mood induction may have attenuated the normal drop in salivary cortisol levels that occurs when subjects are at rest (e.g., Brown et al., 1993). This was examined by comparing the drop in salivary cortisol during the mood induction procedures (time 0 minus time 20) to the drop during the neutral gardening programme, which lasted roughly the same time. The drop in salivary cortisol level during the positive mood induction and the neutral video did differ but not significantly (positive mood, change from baseline, mean 5 2 1.19, S.E.M. 5 0.734; neutral, mean 5 2 2.73, S.E.M. 5 0.890; P 5 0.095). There was no difference in the drop in salivary cortisol between the negative mood induction and the neutral video (negative mood, change from baseline, mean 5 2 2.85, S.E.M. 5 0.687; neutral, mean 5 2 2.73, S.E.M. 5 0.890; P 5 0.918). The drop in salivary cortisol during the
Fig. 2. Change from baseline in salivary cortisol level (6S.E.M.) during positive and negative mood induction procedures, for hypomanic and control subjects. Musical mood inductions ran from approximately 3 to 10 min. One-way ANOVA reveals no differences between four groups at baseline (F(3,44) 5 1.078, P 5 0.37). Open squares, hypomanics, positive mood induction; open circles, hypomanics, negative mood induction; closed squares, controls, positive mood induction; closed circles, controls, negative mood induction.
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positive and negative conditions did differ, but again, the difference was not significant (P 5 0.074). When group, gender, and past depression were considered as between-subjects variables in these analyses, none were found to be significant. Hence mood induction was not found to attenuate the normal drop in salivary cortisol during rest.
3.4. Effects of mood induction procedure on neuropsychological performance One-way ANOVAs testing the effects of mood condition on performance revealed no significant effects of mood on gambling game performance (total number of risky choices) (P 5 0.809), category fluency (P 5 0.921), paced counting (P 5 0.705), and fast counting (P 5 0.509) (see Table 3). There was a significant effect of mood on letter fluency (F(1,39) 5 4.80, P 5 0.035) such that subjects in the negative mood condition produced higher verbal output in 3 min relative to subjects in the positive mood condition. When group (hypomanics, controls) and history of depression were considered as second between-subjects variables in these analyses, there were no significant main effects or interaction terms on any of the neuropsychological variables.
3.5. Associations between personality variables, neuropsychological and neuroendocrine measures A significant correlation was found between number of risky choices on the Gambling game and score on the Manic Depressiveness Scale (Pearson’s r 5 0.35, P 5 0.029), such that individuals with more prior manic-depressive experiences tended to make
more risky choices. The depression subscale of the MDS correlated with gambling performance (r 5 0.40, P 5 0.012) but the mania subscale did not. No other personality variables correlated with neuropsychological performance. Associations between personality variables and salivary cortisol response were examined using summed changes from baseline (at times 10, 15, 20) as a single figure of cortisol response. There were no significant correlations between personality variables and salivary cortisol response during either positive or negative mood inductions.
4. Discussion The aim of the present study was to demonstrate differential effects of induced positive and negative moods in a non-clinical sample on two neuropsychological tests: verbal fluency and the gambling game. Salivary cortisol measures were recorded in an effort to validate the efficacy of the mood inductions. Self-report data from the visual analogue scales and the BFS indicate the positive mood induction achieved a robust effect of elation lasting for the duration of the procedure, whilst the negative mood induction achieved a robust and lasting effect of depression. These contrasting mood states, however, were without major effects at the neuroendocrine and neuropsychological levels. There were no significant differences between salivary cortisol levels during the positive and negative mood inductions. The drop in cortisol levels during the two mood inductions did not significantly differ from the drop in cortisol level whilst subjects
Table 3 Verbal fluency and gambling game performance for hypomanic and control subjects after positive and negative mood induction procedures (MIPs) Hypomanics
Fluency, FAS Fluency, category Paced counting (s) Fast counting (s) Gambling game: risky (AB) choices (%)
Controls
Positive MIP (n 5 10)
Negative MIP (n 5 10)
Positive MIP (n 5 11)
Negative MIP (n 5 10)
41.2 (3.4) 42.5 (3.2) 5.99 (0.68) 1.32 (0.12) 42.3 (3.6)
53.9 (3.9) 40.9 (2.9) 5.85 (0.97) 1.35 (0.09) 40.6 (4.5)
45.9 (4.6) 41.7 (2.4) 5.58 (0.94) 1.22 (0.10) 43.2 (2.1)
49.8 (2.8) 43.8 (1.6) 6.32 (0.61) 1.31 (0.04) 43.1 (3.7)
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watched a gardening video, which is suggested to serve as a neutral mood control condition. These data fail to support the results of Brown et al. (1993) who found a gradual rise in serum cortisol levels in the 60 min subsequent to both positive and negative mood inductions. There is no reason to suppose that fluctuations in serum cortisol levels cannot be detected as easily in salivary samples as in plasma. It is conceivable that the effect on salivary cortisol may not be detectable within the first 10 min subsequent to the mood induction. However, if it were a delayed effect, we would have expected to see it during the subsequent neutral video condition, which was not the case. Alternatively, it may be significant that Brown et al. recorded resting cortisol levels for 135 min prior to the mood induction procedure, allowing the cortisol level to reach its nadir. Whatever the explanation, the results of this study do not support salivary cortisol measurement as a simple and reliable objective method of validating psychological mood induction. It was hypothesised that positive mood would be associated with increased risky decision-making on the Gambling Game, which may be indicative of vPFC involvement in normal and pathological mood processes. The hypothesis was not supported; there were no differences in gambling game performance between positive and negative mood conditions. In the absence of a neutral mood control condition, it is feasible that positive and negative mood both influence decision-making in a similar manner. This is considered unlikely for two reasons. Firstly, our data closely resemble the control data from 44 subjects from the Bechara et al. (1994) original report. Secondly, there is evidence that depressed mood is associated with reduced sensitivity to reward (e.g., Costello, 1972; Henriques et al., 1994); hence depressed subjects should derive less benefit from risky choices, and so we would predict positive and negative induced moods to have opposing effects on gambling game performance. Verbal fluency performance was also examined in relation to positive and negative induced mood, with the hypothesis that positive mood would be associated with higher verbal output that negative mood (Table 3). There were no differences in category fluency performance between mood conditions, and on FAS fluency the opposite effect was found:
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negative mood was associated with higher verbal fluency than positive mood. In the absence of a neutral mood control condition it is impossible to ascertain whether this effect is specific to negative mood or positive mood, or whether the two states have opposing, and counterintuitive, effects on verbal fluency. There are a number of reports indicating verbal fluency is reduced in clinical depression and that it is state dependent (e.g., Trichard et al., 1995), so this finding with mood induction must await replication. In an attempt to maximise the effectiveness of the positive mood induction, a group of subjects with previous subclinical hypomanic experience were recruited. This is a novel approach in research into mania. Subjects with previous hypomanic experience and control subjects showed similar mood shifts on the self-report scales, similar salivary cortisol effects, and performed similarly on the neuropsychological tasks. The hypothesis that the subjects with previous hypomanic experience would show higher susceptibility to positive mood induction was thus refuted. A correlation was revealed between score on the Manic-Depressiveness Scale and risky choices on the gambling game, however. This may represent a trait marker in the hypomanic subjects, associated with riskiness or impulsivity. It does not appear to be influenced by state fluctuations in normal mood. The two subject groups were both recruited using a screening questionnaire adapted from DSM-IV criteria for a hypomanic episode. However, the criteria on the questionnaire required a milder episode than DSM-IV criteria, and there are no previous studies in the literature validating this questionnaire. Eleven subjects in the group with hypomanic experience met formal criteria for Bipolar II Disorder when assessed with the SCID (First et al., 1997), and the group scored significantly higher than controls on the Manic-Depressiveness Scale (Thalbourne et al., 1994), a measure of previous bipolar experiences; and the AIM (Larsen and Diener, 1985), a measure of the tendency to experience extreme rather than mild forms of emotion. These findings lend support to the argument that this group may represent the mild end of the bipolar spectrum. However, none of the subjects in this group had consulted a psychiatrist about their mood, or had received any psychiatric treatment. They must therefore be considered a non-
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clinical sample, and as such, the generalisability of these findings to a clinical sample of bipolar patients is unclear. The authors are unaware of any published studies investigating positive mood induction in bipolar patients, but the present results raise the possibility that bipolar patients would not show an increased susceptibility to positive mood induction and would not manifest a neuropsychological ‘relapse’ under conditions of mood induction. The present findings are critical to the interpretation of neuropsychological studies in pathological mood states. Major depression and mania have both been associated with deficits on neuropsychological tasks sensitive to prefrontal cortex dysfunction (Morice, 1990; Dolan et al., 1994; Beats et al., 1996). It is possible, however, that these impairments are merely a temporary feature of affective disturbance, and prefrontal task performance may be influenced by relatively subtle changes in mood. The present findings, although in a non-clinical sample, indicate this is unlikely. They give weight to the argument that the reported deficits in mood disorder patients are associated with a stable, state-related abnormality in prefrontal cortex and, moreover, that neuropsychological assessments in mood disorder patients provide insight into the underlying neural mechanisms of mood disorder.
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