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Ventromedial prefrontal value signals and functional connectivity during decision-making in suicidal behavior and impulsivity.

ABSTRACT: Suicide is linked to impaired value-based decision-making and impulsivity, but whether these risk factors share neural underpinnings is unclear. Disrupted ventromedial prefrontal cortex (vmPFC) value signals may underlie this behavioral phenotype. We investigated vmPFC value signals, vmPFC-frontoparietal connectivity, and the impact of impulsivity during decision-making in depressed individuals with and without suicidal behavior. Middle-aged and older adults (n?=?116; 35 with a history of suicide attempts, 25 with ideation only, 25 depressed controls with no ideation, and 31 nonpsychiatric controls) completed a decision-making task with drifting reward probabilities during fMRI. Values of choices, estimated by a reinforcement learning model, were regressed against BOLD signal. VmPFC value activation was compared between groups. Moderating effects of impulsivity on vmPFC-frontoparietal connectivity were assessed in nonpsychiatric controls and compared among patient groups. VmPFC value responses in participants with a history of suicide attempts were reduced relative to nonpsychiatric controls (p?FWE corrected?

SUBMITTER: Brown VM

PROVIDER: S-EPMC7162923 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Ventromedial prefrontal value signals and functional connectivity during decision-making in suicidal behavior and impulsivity.

Brown Vanessa M VM Wilson Jonathan J Hallquist Michael N MN Szanto Katalin K Dombrovski Alexandre Y AY

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology 20200208 6

Suicide is linked to impaired value-based decision-making and impulsivity, but whether these risk factors share neural underpinnings is unclear. Disrupted ventromedial prefrontal cortex (vmPFC) value signals may underlie this behavioral phenotype. We investigated vmPFC value signals, vmPFC-frontoparietal connectivity, and the impact of impulsivity during decision-making in depressed individuals with and without suicidal behavior. Middle-aged and older adults (n = 116; 35 with a history of suicid ...[more]

PMID: 32035425

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Project description:RATIONALE:During value-based decision-making, organisms make choices on the basis of reward expectations, which have been formed during prior action-outcome learning. Although it is known that neuronal manipulations of different subregions of the rat prefrontal cortex (PFC) have qualitatively different effects on behavioral tasks involving value-based decision-making, it is unclear how these regions contribute to the underlying component processes. OBJECTIVES:Assessing how different regions of the rodent PFC contribute to component processes of value-based decision-making behavior, including reward (or positive feedback) learning, punishment (or negative feedback) learning, response persistence, and exploration versus exploitation. METHODS:We performed behavioral modeling of data of rats in a probabilistic reversal learning task after pharmacological inactivation of five PFC subregions, to assess how inactivation of these different regions affected the structure of responding of animals in the task. RESULTS:Our results show reductions in reward and punishment learning after PFC subregion inactivation. The prelimbic, infralimbic, lateral orbital, and medial orbital PFC particularly contributed to punishment learning, and the prelimbic and lateral orbital PFC to reward learning. In addition, response persistence depended on the infralimbic and medial orbital PFC. As a result, pharmacological inactivation of the infralimbic and lateral orbitofrontal cortex reduced the number of reversals achieved, whereas inactivation of the prelimbic and medial orbitofrontal cortex decreased the number of rewards obtained. Finally, using simulated data, we explain discrepancies with a previous study and demonstrate complex, interacting relationships between conventional measures of probabilistic reversal learning performance, such as win-stay/lose-switch behavior, and component processes of value-based decision-making. CONCLUSIONS:Together, our data suggest that distinct components of value-based learning and decision-making are generated in medial and orbital PFC regions, displaying functional specialization and overlap, with a prominent role of large parts of the PFC in negative feedback processing.

Project description:The ventromedial prefrontal cortex (vmPFC) and insular cortex are implicated in distributed neural circuitry that supports emotional decision-making. Previous studies of patients with vmPFC lesions have focused primarily on decision-making under uncertainty, when outcome probabilities are ambiguous (e.g. the Iowa Gambling Task). It remains unclear whether vmPFC is also necessary for decision-making under risk, when outcome probabilities are explicit. It is not known whether the effect of insular damage is analogous to the effect of vmPFC damage, or whether these regions contribute differentially to choice behaviour. Four groups of participants were compared on the Cambridge Gamble Task, a well-characterized measure of risky decision-making where outcome probabilities are presented explicitly, thus minimizing additional learning and working memory demands. Patients with focal, stable lesions to the vmPFC (n = 20) and the insular cortex (n = 13) were compared against healthy subjects (n = 41) and a group of lesion controls (n = 12) with damage predominantly affecting the dorsal and lateral frontal cortex. The vmPFC and insular cortex patients showed selective and distinctive disruptions of betting behaviour. VmPFC damage was associated with increased betting regardless of the odds of winning, consistent with a role of vmPFC in biasing healthy individuals towards conservative options under risk. In contrast, patients with insular cortex lesions failed to adjust their bets by the odds of winning, consistent with a role of the insular cortex in signalling the probability of aversive outcomes. The insular group attained a lower point score on the task and experienced more 'bankruptcies'. There were no group differences in probability judgement. These data confirm the necessary role of the vmPFC and insular regions in decision-making under risk. Poor decision-making in clinical populations can arise via multiple routes, with functionally dissociable effects of vmPFC and insular cortex damage.

Dataset Information

Ventromedial prefrontal value signals and functional connectivity during decision-making in suicidal behavior and impulsivity.

Publications

Ventromedial prefrontal value signals and functional connectivity during decision-making in suicidal behavior and impulsivity.

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