Behavioral inhibition system (BIS), Behavioral activation system (BAS) and schizophrenia: Relationship with psychopathology and physiology
Introduction
Gray, 1976, Gray, 1987, Gray, 1994 conceptualized two neural motivational systems that regulate the intensity of approach and withdrawal behaviour in response to environmental stimuli: the Behavioral Activation System (BAS) and the Behavioral Inhibition System (BIS). BAS is hypothesized to control approach behaviour in response to cues of reward via dopaminergic activity in the mesolimbic system (Depue and Collins, 1999, Gray, 1994), whereas BIS is hypothesized to be sensitive to cues of threat and punishment and to activate responses of inhibition and avoidance via noradrenergic and serotonergic activity in the septohippocampal system (Depue and Jacono, 1989, Gray, 1982, Gray, 1994). Recently, Gray’s theory has been adapted, viewing the BIS being distributed among a number of neural structures controlled by the septo-hippocampal system and the amygdala and regarding the BIS as sensitivity to conflicts in general (Gray and McNaughton, 2000, McNaughton and Corr, 2004).
Sensitivity of the BIS/BAS systems is biologically based, while reactivity of the systems is conditioned by environmental input. Therefore, individual differences in risk factors and protective factors (e.g. gender differences in socialization with respect to reward and punishment conditioning) will affect the sensitivity to punishment and reward. Gray’s theory is one of the most influential biologically based personality theories, and has motivated research in the neurophysiological (e.g. Blair, 2003, Coan and Allen, 2003, Cools et al., 2005, Hawk and Kowmas, 2003, Keltinkangas-Järvinen et al., 1999, Reuter et al., 2005, Sutton and Davidson, 1997), and the molecular genetic basis of the BIS and BAS systems (Cools et al., 2005). For instance, this research has shown that BIS scores predict serotonergic modulation of amygdala responses to fearful faces (Cools et al., 2005) and that the interaction of COMT and DRD2 polymorphisms predicts variations in the behavioral approach system (Reuter et al., 2005).
Although there have been previous attempts to measure Gray’s BIS/BAS dimensions, these have all been hampered by considerable conceptual and psychometric problems. Therefore Carver and White (1994) developed a brief questionnaire to measure BIS and BAS sensitivities, focussing mainly on the emotional consequences of BIS/BAS sensitivity. The BIS items assess responsiveness to impending punishing events and the BAS items assess responsiveness to reward (BASR), funseeking (BASF), and drive towards appetitive goals (BASD) in 3 sub-scales. The Carver and White scales are the most comprehensive and specific measure of BIS/BAS sensitivities. Several validation studies found support for the validity of this BIS/BAS scales (Campbell-Sills et al., 2004, Heubeck et al., 1998, Jorm et al., 1999), and showed the generalizability across samples (n = 646) from the USA, UK and Italy (Leone et al., 2001). In clinical studies(Carver et al., 2000, Kasch et al., 2002) BIS/BAS levels, assessed with this questionnaire, proved to be stable over time and clinical state, being more a measure of trait (correlating with measures of personality constructs) than of state (correlating with measures of current clinical symptoms).
Sex differences have been reported for the BIS/BAS scales, with women showing higher sensitivity on the BIS (Leone et al., 2001). Externalizing disorders, including substance abuse and antisocial behaviour, are more frequent in men (Rosenfield, 2000), and have been found to be significantly associated with higher BAS scores (Newman et al., 1997, Newman et al., 2005).
Overactivity and underactivity in the BIS and BAS systems, and relative imbalance between BIS and BAS systems, have been related to risk for various forms of psychopathology (Johnson et al., 2003). For example, depression has been shown to be associated with high sensitivity on the BIS and low sensitivity on the BAS (Kasch et al., 2002), bipolar disorder with both elevated BIS and BAS (Depue and Jacono, 1989, Johnson et al., 2000, Meyer et al., 2001), anxiety disorder (Carver, 2004), nervousness and high levels of internalizing behaviour (Colder and O’Connor, 2004) with high BIS sensitivity, and Attention Deficit Hyperactivity Disorder (ADHD) with low BIS sensitivity (Matthys et al., 1998). Higher sensitivity to reward (BAS) has been suggested to underlie psychopathy, and high levels of externalizing problems (Newman et al., 1997, Newman et al., 2005). Surprisingly, to date, the BIS/ BAS scales have not been investigated in patients with schizophrenia. However, in a study by Berenbaum and Fujita (1994) patients with schizophrenia have been found to show increased neuroticism and decreased extraversion compared to controls. Therefore, we hypothesized patients to show higher sensitivity to punishment (BIS) than control subjects.
Excessive phasic dopaminergic transmission has been suggested to underlie psychotic (positive) symptoms and increased emotional reactivity in schizophrenia (Aleman and Kahn, 2005, Davis et al., 1991). Since the mesolimbic system is involved in behavioral reinforcement and motivation, and since the role of the dopaminergic reward system is to direct attention towards reward-indicating stimuli and to predict reward, excessive dopaminergic transmission may result in over-attribution of meaning to otherwise irrelevant cues. Reduced dopamine receptor sensitivity in the striatum, increased by neuroleptics, is associated with negative symptoms (avolition, apathy, affective flattening) (Heinz et al., 1998) and may reduce motivational and emotional responses to reward-indicating situations. (Robbins and Everitt, 1996, Schultz et al., 1997). Therefore we expected higher sensitivity to reward (BAS) to correspond to high levels of positive symptoms, and lower sensitivity to reward to high levels of negative symptoms.
With regard to sex differences, a recent study by Myin-Germeys et al. (2004) indicated that women with psychotic symptoms reacted more strongly to daily life stress than men, with increase in negative affect and decrease in positive affect. Since women have been found to show higher sensitivity on the BIS (Jorm et al., 1999, Leone et al., 2001), and more internalizing problems than men (Rosenfield, 2000), we also expected women with schizophrenia to be more sensitive to threat (i.e., elevated BIS scores) than men with schizophrenia.
Several studies have reported increased average heart rate (HR) (Rechlin et al., 1994, Rechlin, 1995, Zahn et al., 1981a, Zahn et al., 1981b, Zahn et al., 1997) and decreased heart rate variability (HRV) (Bär et al., 2005), in patients with schizophrenia. Since increased HR and decreased HRV have been shown to correlate with inhibited behaviour (Kagan et al., 1987, Kagan et al., 1988, Reznick et al., 1986) these psychophysiological measures were also obtained. We expected high BIS sensitivity to correlate with high scores on average heart rate (HR), and with low scores on heart rate variability (HRV).
Section snippets
Participants
Forty-two patients with schizophrenia (26 men, 16 women) and 37 healthy controls (17 men, 20 women) participated in this study.
All patients were recruited from the Schizophrenia Research Unit of the Utrecht University Hospital. Most patients (n = 40) were outpatients. Some of them had been hospitalized for a first psychosis or a relapse for several weeks, others visited the clinic for a second opinion or received treatment on an outpatient basis for several months. Psychiatric diagnosis was
Clinical variables
As can be seen in Table 1, no significant differences were found in the patient groups between men and women in severity of negative symptoms, positive symptoms and general psychopathology sub-scale, measured by the PANSS.
BIS
A 2 × 2 ANOVA (Group, Sex) on all BIS items revealed a significant effect of Group (F(df 1,75) = 4.7; p = 0.034), controls showing less sensitivity than patients, and of Sex (F(df 1,75) = 5.1; p = 0.026), men showing less sensitivity than women. There was no interaction.
No correlations
Discussion
This study examined sensitivity to punishment (BIS) and reward (BAS) in patients with schizophrenia compared to controls. In addition, we analyzed psychophysiological measures of average heart rate (HR) and heart rate variability (HRV) in both groups.
Patients showed a higher sensitivity to threat than controls. This higher BIS sensitivity correlated with longer duration of illness and lower scores on the negative PANSS symptoms. Higher BIS sensitivity has also been reported in anxiety disorder,
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2021, Learning and MotivationCitation Excerpt :Gray’s theory was groundbreaking in the field of personality and some researchers created instruments that encompassed the concepts of his theory (Torrubia, Ávila, Moltó, & Caseras, 2001; Wilson, Gray, & Barrett, 1990). Carver and White designed the BIS/BAS scale in the early 1990s, and it is probably the most widely used instrument in the field of psychology (Carver & White, 1994; Scholten, Honk, Aleman, & Kahn, 2006). To assess the BIS the person has to answer, on a 4-points likert-scale, statements about potentially punishing events, while to assess the BAS the statements refer to potentially rewarding events.
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2018, Personality and Individual DifferencesCitation Excerpt :Activation of the BIS is related to neuroticism and anxiety traits, and activation of the BAS is related for extraversion, novelty seeking, reward dependence and openness to experience (Kennis, Rademaker, & Geuze, 2013). The BIS and BAS have been studied in relation to psychopathology, such as depression (Kasch, Rottenberg, Arnow, & Gotlib, 2002), social anxiety (Kimbrel et al., 2016) and schizophrenia (Scholten, van Honk, Aleman, & Kahn, 2006). Gray's (1991) theory of BIS/BAS offers an adequate view of personality that may be especially relevant to changes associated with PD, MS and ST symptoms.