the functioning of the behavioral activation and inhibition systems in bipolar i euthymic patients...

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Personality and Individual Differences 42 (2007) 1323–1331

The functioning of the Behavioral Activation and InhibitionSystems in bipolar I euthymic patients and its influencein subsequent episodes over an eighteen-month period

Jose Salavert a,b,d, Xavier Caseras b,*, Rafael Torrubia b, Sandra Furest c,Belen Arranz d, Rosa Duenas a, Luis San d

a Benito Menni CASM, Barcelona, Catalonia, Spainb Institut de Neurociencies de la UAB, Departament de Psiquiatria i Medicina Legal,

Universitat Autonoma de Barcelona, Catalonia, Spainc Unitat d’Estudi del Comportament, Hospital Materno-infantil de la Vall d’Hebron,

Unitat de Paidopsiquiatria, Barcelona, Catalonia, Spaind Unidad Integrada de Psiquiatrıa Hospital Vall d’Hebron – Hospital San Rafael, Barcelona, Catalonia, Spain

Received 10 May 2006; received in revised form 14 August 2006; accepted 3 October 2006Available online 28 November 2006

Abstract

In order to better understand individual vulnerabilities to bipolar I disorder, this study evaluates indi-vidual differences in Behavioral Activation and Inhibition Systems as possible markers of bipolar I disor-der. BAS and BIS functioning was evaluated in 39 bipolar I euthymic patients and in 38 controls. Patientsshowed higher scores on the BAS scale; differences were not detected on the BIS scale. Eighteen monthspost-initial assessment, patients were re-grouped according to the presence and type of new episodes.Patients relapsing with a depressive episode showed lower scores on the BAS scale than patients sufferingfrom a manic/hypomanic episode, and a tendency to score lower than patients still asymptomatic. Reportedhigher BAS functioning would reinforce the hypothesis of a trait vulnerability to present approach behav-iors during euthymia associated with bipolar I disorder, not necessarily related to the proximity of a manic/hypomanic episode, and interestingly not detected when approaching a depressive episode, circumstance in

0191-8869/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.doi:10.1016/j.paid.2006.10.010

* Corresponding author. Present address: Institute of Psychiatry, Section of Neuroscience and Emotion, PO69,De Crespigny Park, Denmark Hill, London SE5 8AF, UK. Tel.: +44 2078480659; fax: +44 2078480379.

E-mail address: [email protected] (X. Caseras).

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1324 J. Salavert et al. / Personality and Individual Differences 42 (2007) 1323–1331

which BAS functioning would be similar to controls. Results did not reveal a weaker BIS in patients,hypothesized to account for BAS instability in bipolar I disorder.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Bipolar I disorder; Behavioral activation system; Behavioral inhibition system; BAS; BIS

1. Introduction

Although bipolar disorders are highly social and occupationally disabling conditions, associ-ated with a high suicide risk (30 times greater than those without a mood disorder) and a veryhigh cost to health systems (Davidson et al., 2002), few studies have been devoted to the under-standing of underlying neurobehavioral factors, which could explain, in part, individual vulnera-bilities to suffering from this condition.

Depue and colleagues (Depue & Iacono, 1989; Depue & Zald, 1993) have proposed a neurobe-havioral model for bipolar disorders. Following these authors, a Behavioral Facilitation System(BFS) would be responsible for behavioral activation in response to a broad range of stimuluscontext, including a reward-acquisition component. This system would be based on dopaminepathways of the ventral tegmental area, running through the nucleus accumbens and projectingon prefrontal regions. A high reactive BFS would respond to minimal environmental incentives,resulting in a great number of exploratory and approach behaviors, and in a high tendency topresent positive affective states (curiosity, desire, hope, euphoria, or excitation). According to this,depressive symptoms may reflect a deficient activity of the BFS, whereas hypomanic/manic symp-toms may result from an excessively high activity of the same system. Bipolar patients would showa weak regulatory strength of the BFS, showing a vulnerability to episodes of extreme engagementor disengagement of this system.

The similarities between the BFS proposed by Depue and colleagues and the Behavioral Acti-vation System (BAS) proposed by Gray (1981) are remarkable, not only in their general concep-tion, but also in their triggers, functioning, outputs and neuroanatomical bases. However, Grayalso described the Behavioral Inhibition System (BIS), responsible for behavioral stop and real-location of attention in response to aversive or novel stimuli. The BAS or the BIS will take over(control mode) behavior, respectively, when positive or negative cues are faced, resulting in theinhibition of the other system. Individuals with an overactive BIS would have a greater probabil-ity of inhibiting appetitive responses when faced with a punishing stimulus than those with anunderactive BIS. Similarly, individuals with an overactive BAS have a greater probability ofapproaching towards a rewarding stimulus than those with an underactive BAS. Furthermore,the BIS will work as a comparator (checking mode); that is, analyzing incoming stimuli in relationto previous experiences. If the present stimulus has been previously associated with negative expe-riences, the comparator would lead to the BIS taking control over the behavior; if the stimulus hasbeen previously associated with reward, the BAS would prevail over the BIS. Gray also proposedthat the BAS could also work in checking mode (Gray & Smith, 1969). Unlike when working incontrol mode, during checking mode the functioning of the BIS and the BAS is independent.

Analogously to Depue, Fowles (1993) has proposed that BAS would be hyperactive in manicpatients. However, he has not suggested any mechanism to explain a BAS deregulation which

J. Salavert et al. / Personality and Individual Differences 42 (2007) 1323–1331 1325

would account for the occurrence of successive manic and depressive episodes in bipolar patients.In this sense, we can hypothesize that a weak BIS would fail in its role of comparator; in otherwords, it would fail to predict the consequences of the presented stimuli. Because of this, theengagement of BAS would occur randomly.

To our knowledge only one study (Meyer, Johnson, & Winters, 2001) has looked at the func-tioning of BIS and BAS in bipolar patients. The authors found a significant positive correlationbetween the BIS scale and severity of depressive symptoms, but no significant correlation betweenthis scale and the severity of manic symptoms. The BAS scale did not correlate with the severity ofeither depressive or manic symptoms. However, the lack of a control group and the fact that pa-tients were symptomatic (either depressed or manic) when completing the BIS/BAS scales (thepresence of affective symptoms easily affects scores on personality traits), constitute one of themajor caveats of this study.

The present study aimed to evaluate the functioning of the BAS and BIS in euthymic bipolarpatients, and to compare them against a control group with similar socio-geographic characteris-tics. We were also interested in studying the relationship between the functioning of the BAS andBIS during euthymia and the polarity of possible subsequent episodes.

2. Methods

2.1. Participants

A total of 77 participants were included in this study (39 bipolar I outpatients and 38 healthycontrols). Patients were selected from those attending follow-up sessions at the Benito MenniMental Health Institute, after being included in treatment for bipolar I disorder (Bp I). Patientsattended the out-patients unit once every 2 months as average for controls on their treatmentcompliance and to receive reinforcement of the medical advice and prescriptions; eventually bloodtests were also carried out. At the moment of their inclusion 26 patients were following a main-tenance program with lithium, 9 with valproate, 3 oxcarbazepine and 1 carbamazepine. Includingcriteria were (a) positive Bp I diagnosis according to DSM-IV and ICD-10 diagnostic criteria, (b)score 67 on the Hamilton depression rating scale (HAM-D); (c) score 66 on the Young maniarating scale (YMRS); and (d) absence of substance abuse. The healthy control sample was selectedfrom non-first degree patients’ relatives (13% of the final sample) and staff from the institutionwhere the study took place, all of whom (a) came from the same socio-geographic area as theBp I patients included in the study, (b) reported no current or past psychiatric disorder, (c) werenot currently taking any psychotropic medication, (d) scored 67 on the HAM-D, and (e) scored66 on the YMRS.

2.2. Procedure

Patients included in this study had previously received a diagnosis of Bp I and were included ina maintenance follow-up program. At the moment of their inclusion in the study, some patientshad only been asymptomatic in the maintenance program for 4 months and some others for aslong as 36 months (mean = 10.75, sd = 8.34). A second diagnosis was obtained from an external


and experienced psychiatrist by means of a checklist including DSM-IV and ICD-10 for Bp I. Thissecond diagnosis was based on interviews with patients and with their relatives, as well as consul-tation of patient files. The inclusion of patients in the study was subjected to Bp I diagnostic con-cordance between the initial and the present assessment (kappa obtained = 0.846). Presenteuthymic state was also subjected to the concordance between diagnosis and scores on theHAM-D and the YMRS. From the 43 patients initially evaluated, 3 were excluded due to scoresover the selected cut-off in the HAM-D and/or the YMRS, and 1 because of a lack of diagnosticconcordance.

The same experienced psychiatrist screened control participants following a DMS-IV criteriachecklist including anxiety, affective and psychotic disorders, and included them in the study onlyif no past history of, or current psychopathology was detected, and their scores on the HAM-Dand the YMRS were within the pre-defined range.

Eighteen months after their inclusion in the study, each patient’s file was revised in order torecord any possible new affective episode suffered.

2.3. Instruments

Participants’ emotional state was measured by means of the Spanish versions of the HAM-D(Ramos-Brieva & Cordero, 1986) and YMRS (Marcos, 1997). The former is a validated versionof the original 17-item HAM-D (Hamilton, 1960), and the latter of the original 11-item YMRS(Young, Biggs, Ziegler, & Meyer, 1978). Both measures are clinician-rating instruments.

The functioning of the BIS and BAS was assessed by means of the original Spanish version ofthe Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) (Torrubia, Avila,Molto, & Caseras, 2001). This self-reported questionnaire is made up of 48 yes/no items, dividedin two scales. The Sensitivity to Punishment scale (SP) evaluates individual differences in BISfunctioning, and the Sensitivity to Reward scale (SR) evaluates individual differences in BAS func-tioning. Both scales include items depicting control and checking modes of functioning, areorthogonal and have shown good psychometric properties (Brebner, 1998; Brebner & Martin,1995; Caseras, Avila, & Torrubia, 2003; Torrubia et al., 2001; Zuckerman, 1999; Zuckerman, Joir-eman, Kraft, & Kuhlman, 1999). Several laboratory studies have also confirmed the validity of thetwo scales in predicting different types of disinhibited behavior related with the functioning ofthese systems in checking and control modes (ex. Avila, 2001; Avila & Torrubia, 2006; Torrubia,Avila, Molto, & Grande, 1995).

2.4. Analyses

Comparisons between groups in socio-demographic variables were computed by means of Stu-dent’s t-test or chi-square, as appropriate. HAM-D and YMRS scores were compared betweengroups by means of the Mann–Whitney U-test, and scores on the SP and SR scales by meansof Student’s t-test. A logistic regression with group as dependent variable and symptoms and traitscales as predictors was conducted in order to further study the relationship between these scalesand group membership.

After an 18 month period, participants were re-grouped regarding the polarity of the first epi-sode (if any) presented after their inclusion in this study. Comparisons between manic/hypomanic,


depressed and asymptomatic patients on their initial scores on the SP and SR scales were con-ducted by means of ANOVAs and by means of Kruskal–Wallis in the case of YMRS andHAM-D.

3. Results

Patients and controls were not different in mean age (mean = 38.76, SD = 14.59 for patients,and mean = 34.18, SD = 10.71 for controls; t(75) = 1.56, p > .1), gender distribution (femaleswere 59% in the patients group and 50% in the controls; v2(1) = 0.62, p > .1) or educational level(few participants had received higher education either in the patient or the control group;v2(2) = 1.75; p > .1). As expected, there were differences in employment status (v2(2) = 16.66;p < 0.001), with more active workers in the control group. The length of time asymptomatic be-fore inclusion in the study did not correlate with any of the scales used (i.e., SP, SR, HAM-D andYMRS; all p > .1).

Patients showed a median score of 1 (range 0–5) on the HAM-D, and of 2 (range 0–5) on theYMRS. Controls’ median score was 0 on the HAM-D (range 0–3) and 1 on the YMRS (range 0–4). Comparing these scores between patients and controls, there were no significant differenceseither for the HAM-D (U = 590, p > .1), or the YMRS (U = 598.5, p > .1). Scores on the SP scalewere not different between patients (mean = 10.46, SD = 5.29) and controls (mean = 8.68,SD = 5.09), t(75) = 1.50, p > .1; whereas on the SR scale, patients (mean = 11.90, SD = 4.44)showed higher scores than controls (mean = 7.16, SD = 3.79), t(75)=5.02, p < 0.001.

When including HAM-D, YMRS, SP and SR scores as predictors of group membership in alogistic regression analysis, only SR showed to be significant (B = �0.271, p < .001, Odds

Table 1Scores on symptoms and trait scales for those patients who relapsed with a new depressive or manic/hypomanic episodeduring the eighteen-month follow-up, and those who did not

Asymptomatic after 18 months Not asymptomatic after 18 monthsNo affective episodes Type of first affective episode

Manic/hypomanic Depressive

Mean (SD)

SR 11.76 (3.71) 13.78 (4.68) 8.29 (3.94)SP 10.47 (5.17) 9.11 (5.57) 11.14 (6.04)

Median (range)

HAM-D 1 (0–3) 1 (0–3) 0 (0–4)YMRS 2 (0–3) 2 (1–5) 0 (0–3)

Scores included in this table were obtained at the moment of inclusion in this study; i.e. when all participants wereasymptomatic. Comparisons between groups across scales resulted in significant differences between those relapsingwith a depressive episode and those relapsing with a manic/hypomanic episode (p < 0.05). A tendency towards sig-nificant differences was found between the same for the YMRS scale (p = 0.07), and between asymptomatic patientsand those relapsing with a depressive episode for the SR scale (p = 0.06).SR = Sensitivity to Reward; SP = Sensitivity to Punishment; HAM-D = Hamilton depression rating scale; YMR-S = Young mania rating scale.


Ratio = 0.763). This was also the case when the interaction SP · SR was also included in the anal-ysis. SR accounted for most of the variance explained by the interaction term, which was not sig-nificant after SR entered the equation (p > .1).

Eighteen months after their inclusion in the study, 22 patients had suffered from at least onenew affective episode. Of these, nine suffered from a manic/hypomanic episode, six suffered froma mixed episode, and seven from a depressive episode. There were no differences on SP scoresacross patients suffering from a new depressive episode, patients relapsing with a manic/hypo-manic episode and those still asymptomatic, F(2,30) = 0.30, p > .1. However, differences acrossgroups emerged when analyzing SR scores, F(2,30) = 3.67, p < .05. Pairwise comparisons showedthat patients relapsing with a new manic/hypomanic episode had obtained at intake higher SRscores than those relapsing with a depressive episode (p < .05). The latter group also approachedsignificance (p = .06) showing lower scores than patients still asymptomatic. Groups did not showdifferences on their initial scores on HAM-D (v2(2) = 0.41, p > .1) or on YMRS (v2(2) = 5.30,p = .07), even though on the latter scale there was a tendency towards significance (Table 1).

4. Discussion

As hypothesized after the proposals by Depue and Iacono (1989), Depue and Zald (1993) andFowles (1993), asymptomatic Bp I patients showed a higher BAS activity (indexed by means ofthe SR scale) than controls. Moreover, the score obtained on the BAS functioning scale was morepredictable of group membership (Bp I vs. control) than the score on any of the other scales usedin this study (including the YMRS). This would reflect a trait vulnerability to overreact or engagein excessive approach behaviors in response to positive stimuli, as well as a greater predispositionto positive affective states. These characteristics would occasionally be exacerbated, making it pos-sible to then consider the presence of a manic episode. The present results are in accordance withthe higher levels of inter-episodic impulsivity in bipolar patients reported by Swann, Anderson,Dougherty, and Moeller (2001), and with the elevations observed in the Reward Dependence(RD) and Novelty Seeking (NS) scales of the TPQ questionnaire, published by Osher, Cloninger,and Belmaker (1996) and Young et al. (1995), respectively.

However, we have not found differences in the functioning of the BIS (indexed by means of theSP scale) which could explain the emotional instability shown by Bp I patients (i.e., alternation ofdepressive and manic episodes). We hypothesized that a weak BIS would lead to a more unstableBAS. A weaker BIS would not be able to inhibit BAS activation in a context where signals forreward and punishment could appear together, resulting in excessive approach behaviors in thosehaving a higher active BAS. Moreover, a weak BIS functioning as a comparator would result in adeficient prediction of expected consequences and could lead to random BAS engagement (i.e.,higher instability in approach responses), resulting in alternate high and low mood episodes.However, this hypothesis is not corroborated by the results obtained in the present paper.

Rather than a higher trait characteristic, the higher BAS functioning score in our Bp I patientssample could suggest that our patients were at the moment of the evaluation more vulnerable tosuffering from a new manic/hypomanic episode, but their scores on the YMRS, with no significantdifferences compared to controls, did not seem to support this. To further study this hypothesis,we recorded the type of their first affective episode, if any, during the eighteen months that fol-


lowed their assessment. Those suffering from a new depressive episode obtained lower scores onthe BAS related scale than those either suffering from a new manic/hypomanic episode or stilleuthymic. At the moment of their assessment, however, patients suffering a new depressiveepisode were observed to have similar scores on the BAS scale than the healthy controls, whereasthose suffering from a new manic/hypomanic episode or still euthymic after eighteen monthsobtained higher scores than the control group. This seems to support the hypothesis of a higherBAS activity trait in Bp I patients, not necessarily related to the proximity of a future manic/hypo-manic episode. However, this higher BAS functioning would not be detected when patientswere approaching a new depressive episode. Interestingly, their scores would not then be lower,but similar to healthy controls. This is in contradiction with previous research conducted with pa-tients suffering from unipolar depression, where a lower BAS functioning compared to controlshas been shown, either when depressed or during euthymia (Kasch, Rottenberg, Arnow, &Gotlib, 2002; Pinto-Meza et al., 2006). The present results could support the claim that unipolarand bipolar depressions are different entities (Hantouche & Akiskal, 2005), suggesting that theywill show different vulnerabilities regarding the functioning of neurobehavioral systems. Whereasunipolar depression seems to be associated with an underactive BAS regardless of the symptom-atic status, patients suffering from bipolar depression will not differ from controls during euthy-mia. Very little research has been conducted looking into differences in vulnerability factors forunipolar and bipolar depression and that conducted has proven inconclusive (Modell, Huber,Holsboer, & Lauer, 2003). Although still tentative, the study of differences in BAS functioningas a vulnerability marker for bipolarity or unipolarity could shed light on this emerging area ofresearch.

One of the major caveats of the present paper is the small sample size. Few patients were able tobe included in the post-eighteen month depressive or manic groups. A longer follow-up period oftime or a larger initial sample size might have produced more conclusive results. However, the factthat with a small sample it is still possible to find significant differences and clear tendencies tosignificance in the sense of the established hypothesis, lends credence to the effects found. Never-theless, more research is needed in order to support the higher BAS activity reported in the presentpaper and to clarify the mechanism related with the possible instability of this system. Larger sam-ples would also facilitate the investigation of the role of BIS in bipolar disorder. It is also impor-tant to take into account that patients in the present study were receiving pharmacologicaltreatment at the moment of their inclusion. That could make the results difficult to generalizeto unmedicated patients or those receiving a different treatment. However, the treatment receivedby our patients was the most common medication in maintenance programs for bipolar patients.Moreover, because of chronicity most bipolar patients are maintained medicated for long-termperiods. Thus, our sample could be considered representative of this type of population. Finally,it could also be helpful to psychometrically distinguish between BIS functioning as a ‘‘compara-tor’’ or in ‘‘control mode’’, although to our knowledge no psychometric instrument has been de-vised to allow this distinction. We are confident that the SP scale used in the present paper, asshown in previous studies (eg. Avila & Torrubia, 2006), allowed for the assessment of BIS inchecking mode. However, this assessment also included the functioning of the BIS in controlmode. To specifically distinguish between both modes of functioning would help to better under-stand processes involved in the hypothesized random over and under activation of the BAS inbipolar patients.


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