Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making

Floresco, Stan; Onge, Jennifer R. St.; Ghods-Sharifi, Sarvin; Winstanley, Catharine A.

doi:10.3758/cabn.8.4.375

Cited by 268 publications

(237 citation statements)

References 101 publications

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“…Clinical and preclinical data suggest that the orbitofrontal cortex (OFC) and basolateral amygdala (BLA) are critically important in mediating cost-benefit decision making (Holland and Gallagher, 2004;Floresco et al, 2008). Although both the BLA and OFC share many reciprocal connections, contradictory reports regarding the effects of damage to these regions has lead to ambiguity concerning their precise contribution to this multifaceted process.…”

Section: Introductionmentioning

confidence: 99%

Lesions of the Basolateral Amygdala and Orbitofrontal Cortex Differentially Affect Acquisition and Performance of a Rodent Gambling Task

Zeeb¹,

Winstanley²

2011

J. Neurosci.

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135

115

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Risky decision making on the Iowa Gambling Task (IGT) has been observed in several psychiatric disorders, including substance abuse, schizophrenia, and pathological gambling. Such deficits are often attributed to impaired processing within the orbitofrontal cortex (OFC) because patients with damage to this area or to the amygdala, which is strongly interconnected with the OFC, can likewise show enhanced choice of high-risk options. However, whether damage to the OFC or amygdala impairs subjects' ability to learn the task, or actually affects the decision-making process itself, is currently unclear. To address these issues, rats were trained to perform a rodent gambling task (rGT) either before or after bilateral excitotoxic lesions to the basolateral amygdala (BLA) or OFC. Maximum profits in both the rGT and IGT are obtained by favoring smaller rewards associated with lower penalties, and avoiding the tempting, yet ultimately disadvantageous, large reward options. Lesions of the OFC or BLA made before task acquisition initially impaired animals' ability to determine the optimal strategy, but did not disrupt decision making in the long term. In contrast, lesions of the BLA, but not the OFC, made after the task had been acquired increased risky choice. These results suggest that, although both regions contribute to the development of appropriate choice behavior under risk, the BLA maintains a more fundamental role in guiding these decisions. The maladaptive choice pattern observed on the IGT in patients with OFC lesions could therefore partially reflect a learning deficit, whereas amygdala damage may give rise to a more robust decision-making impairment.

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Section: Introductionmentioning

confidence: 99%

Lesions of the Basolateral Amygdala and Orbitofrontal Cortex Differentially Affect Acquisition and Performance of a Rodent Gambling Task

Zeeb¹,

Winstanley²

2011

J. Neurosci.

Self Cite

135

115

View full text Add to dashboard Cite

show abstract

“…One key mechanism of DA homeostasis is its reuptake from the synaptic cleft into presynaptic nerve terminals by the DA transporter (DAT). Because several studies support an important role of DA in regulating risk-based decision making in rodents (Floresco et al, 2008;St Onge and Floresco, 2009), altered DAT functioning may contribute to abnormal decision making in individuals with BD. Supporting this assumption, polymorphisms in the DAT gene have been linked with BD (Greenwood et al, 2006;Pinsonneault et al, 2011), likely lowering functional DAT levels (Horschitz et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…Neural networks contributing to decision making have been identified (Floresco et al, 2008;Lin et al, 2008). Clarification of the mechanism(s) underlying decision making in psychiatric patients requires delineation for targeted therapeutic development.…”

Section: Introductionmentioning

confidence: 99%

Reduced Dopamine Transporter Functioning Induces High-Reward Risk-Preference Consistent with Bipolar Disorder

Enkhuizen

Henry

Minassian

et al. 2014

Neuropsychopharmacol

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Individuals with bipolar disorder (BD) exhibit deleterious decision making, negatively impacting their lives. Such aberrant decision making can be quantified using the Iowa Gambling Task (IGT), which requires choosing between advantageous and disadvantageous options based on different reward/punishment schedules. The mechanisms underlying this behavioral deficit are unknown, but may include the reduced dopamine transporter (DAT) functioning reported in BD patients. Using both human and mouse IGTs, we tested whether reduced DAT functioning would recreate patterns of deficient decision making of BD patients. We assessed the IGT performance of 16 BD subjects (7 female) and 17 healthy control (HC) subjects (12 female). We recorded standard IGT performance measures and novel post-reward and post-punishment decision-making strategies. We characterized a novel single-session mouse IGT using C57BL/6J mice (n ¼ 44). The BD and HC IGT performances were compared with the effects of chronic (genetic knockdown (KD; n ¼ 31) and wild-type (n ¼ 28) mice) and acute (C57BL/6J mice (n ¼ 89) treated with the DAT inhibitor GBR12909) reductions of DAT functioning in mice performing this novel IGT. BD patients exhibited impaired decision making compared with HC subjects. Both the good-performing DAT KD and GBR12909-treated mice exhibited poor decision making in the mouse IGT. The deficit of each population was driven by highreward sensitivity. The single-session mouse IGT measures dynamic risk-based decision making similar to humans. Chronic and acute reductions of DAT functioning in mice impaired decision-making consistent with poor IGT performance of BD patients. Hyperdopaminergia caused by reduced DAT may impact poor decision making in BD patients, which should be confirmed in future studies.

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“…These subregions play a pivotal role in economic behavior and decision making as part of the cortico-mesolimbic circuit involving the orbitofrontal cortex (OFC) and the nucleus accumbens (NAc) (14,(19)(20)(21). In rodents, the BLA has been proposed to subserve calculated instrumental behavior, whereas the CMA subserves affective-impulsive behaviors (14,19).…”

mentioning

confidence: 99%

Generous economic investments after basolateral amygdala damage

Honk

Eisenegger

Terburg

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Contemporary economic models hold that instrumental and impulsive behaviors underlie human social decision making. The amygdala is assumed to be involved in social-economic behavior, but its role in human behavior is poorly understood. Rodent research suggests that the basolateral amygdala (BLA) subserves instrumental behaviors and regulates the central-medial amygdala, which subserves impulsive behaviors. The human amygdala, however, typically is investigated as a single unit. If these rodent data could be translated to humans, selective dysfunction of the human BLA might constrain instrumental social-economic decisions and result in more impulsive social-economic choice behavior. Here we show that humans with selective BLA damage and a functional central-medial amygdala invest nearly 100% more money in unfamiliar others in a trust game than do healthy controls. We furthermore show that this generosity is not caused by risk-taking deviations in nonsocial contexts. Moreover, these BLA-damaged subjects do not expect higher returns or perceive people as more trustworthy, implying that their generous investments are not instrumental in nature. These findings suggest that the human BLA is essential for instrumental behaviors in socialeconomic interactions.economic trust | altruism

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Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making

Cited by 268 publications

References 101 publications

Lesions of the Basolateral Amygdala and Orbitofrontal Cortex Differentially Affect Acquisition and Performance of a Rodent Gambling Task

Lesions of the Basolateral Amygdala and Orbitofrontal Cortex Differentially Affect Acquisition and Performance of a Rodent Gambling Task

Reduced Dopamine Transporter Functioning Induces High-Reward Risk-Preference Consistent with Bipolar Disorder

Generous economic investments after basolateral amygdala damage

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