Decision-making and trait impulsivity in bipolar disorder are associated with reduced prefrontal regulation of striatal reward valuation

Liam Mason,Wael El-Deredy,Richard P Bentall,Noreen O’Sullivan,Daniela Montaldi

doi:10.1093/brain/awu152

Liam Mason, Wael El-Deredy + Show 3 more

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https://doi.org/10.1093/brain/awu152

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Journal: Brain	Publication Date: Jun 24, 2014
Citations: 82	License type: cc-by

Affiliation: University of Manchester, University of Liverpool

Abstract

Bipolar disorder is characterized by impaired decision-making captured in impulsivity and risk-taking. We sought to determine whether this is driven by a failure to effectively weight the lower-order goal of obtaining a strongly desired reward in relation to higher-order goals, and how this relates to trait impulsivity and risk-taking. We hypothesized that in bipolar disorder the weighting of valuation signals converging on ventromedial prefrontal cortex are more heavily weighted towards ventral striatum inputs (lower-order), with less weighting of dorsolateral prefrontal cortex inputs (higher-order). Twenty euthymic patients with bipolar disorder not in receipt of antipsychotic medication and 20 case-matched controls performed a roulette task during functional magnetic resonance imaging. Activity in response to high-probability (‘safe’) and low-probability (‘risky’) prospects was measured during both anticipation, and outcome. In control subjects, anticipatory and outcome-locked activity in dorsolateral prefrontal cortex was greater for safe than risky reward prospects. The bipolar disorder group showed the opposite pattern with preferential response to risky rewards. This group also showed increased anticipatory and outcome-locked activity in ventral striatum in response to rewards. In control subjects, however, ventromedial prefrontal activation was positively associated with both ventral striatum and dorsolateral prefrontal activity; patients evidenced a strong positive association with ventral striatum, but a negative association with dorsolateral prefrontal cortex. Response to high-probability rewards in dorsolateral prefrontal cortex was inversely associated with trait impulsivity and risk-taking in the bipolar disorder group. Our findings suggest that clinically impulsive and risky decision-making are related to subjective valuation that is biased towards lower-order preference, with diminished integration of higher-order goals. The findings extend a functional neuroanatomical account of disorders characterized by clinically impulsive decision-making, and provide targets for evaluating interventions that foster self-control.

Highlights

Impulsive and risky decision-making is characteristic of several psychiatric disorders including substance dependence (Rogers et al, 2010), bipolar disorder (Swann et al, 2009), attention deficit hyperactivity disorder (Scheres et al, 2010), pathological gambling (Rogers et al, 2010) and psychopathy (Vitacco and Rogers, 2001)
Whereas longer-term goals are represented in dorsolateral prefrontal cortex (PFC) and lower-order preference in ventral striatum, ventromedial PFC has been proposed to integrate these signals into a weighted valuation that drives subsequent behaviour (Plassmann et al, 2006)
Our findings suggest that in bipolar disorder, and potentially other disorders characterized by impulsivity, the weighting of these signals may be biased towards the ventral striatal contribution, and away from the dorsolateral PFC signal

Summary

Introduction

Impulsive and risky decision-making is characteristic of several psychiatric disorders including substance dependence (Rogers et al, 2010), bipolar disorder (Swann et al, 2009), attention deficit hyperactivity disorder (Scheres et al, 2010), pathological gambling (Rogers et al, 2010) and psychopathy (Vitacco and Rogers, 2001). The nucleus accumbens, part of the ventral striatum, has been shown to code both probability and delay features of rewards indiscriminately, pointing towards a common ‘neural currency’ (Peters and Buchel, 2009). This region responds preferentially to (i) low-probability rewards that are betterthan-expected and so more subjectively gratifying (Yacubian et al, 2006; Smith et al, 2009); and (ii) immediate rewards over those that are superior in the longer-term (McClure et al, 2004). Underlying the role of the dorsolateral PFC in decision-making is its central ability to detect and direct attention towards goal- or task-relevant stimuli (Banich et al, 2000; MacDonald et al, 2000)

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