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Lateral prefrontal model-based signatures are reduced in healthy individuals with high trait impulsivity.

ABSTRACT: High impulsivity is an important risk factor for addiction with evidence from endophenotype studies. In addiction, behavioral control is shifted toward the habitual end. Habitual control can be described by retrospective updating of reward expectations in 'model-free' temporal-difference algorithms. Goal-directed control relies on the prospective consideration of actions and their outcomes, which can be captured by forward-planning 'model-based' algorithms. So far, no studies have examined behavioral and neural signatures of model-free and model-based control in healthy high-impulsive individuals. Fifty healthy participants were drawn from the upper and lower ends of 452 individuals, completing the Barratt Impulsiveness Scale. All participants performed a sequential decision-making task during functional magnetic resonance imaging (fMRI) and underwent structural MRI. Behavioral and fMRI data were analyzed by means of computational algorithms reflecting model-free and model-based control. Both groups did not differ regarding the balance of model-free and model-based control, but high-impulsive individuals showed a subtle but significant accentuation of model-free control alone. Right lateral prefrontal model-based signatures were reduced in high-impulsive individuals. Effects of smoking, drinking, general cognition or gray matter density did not account for the findings. Irrespectively of impulsivity, gray matter density in the left dorsolateral prefrontal cortex was positively associated with model-based control. The present study supports the idea that high levels of impulsivity are accompanied by behavioral and neural signatures in favor of model-free behavioral control. Behavioral results in healthy high-impulsive individuals were qualitatively different to findings in patients with the same task. The predictive relevance of these results remains an important target for future longitudinal studies.

SUBMITTER: Deserno L

PROVIDER: S-EPMC4930122 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Lateral prefrontal model-based signatures are reduced in healthy individuals with high trait impulsivity.

Deserno L L Wilbertz T T Reiter A A Horstmann A A Neumann J J Villringer A A Heinze H-J HJ Schlagenhauf F F

Translational psychiatry 20151013

High impulsivity is an important risk factor for addiction with evidence from endophenotype studies. In addiction, behavioral control is shifted toward the habitual end. Habitual control can be described by retrospective updating of reward expectations in 'model-free' temporal-difference algorithms. Goal-directed control relies on the prospective consideration of actions and their outcomes, which can be captured by forward-planning 'model-based' algorithms. So far, no studies have examined behav ...[more]

PMID: 26460483

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Project description: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.

Project description:BackgroundBehavioral and cognitive control are vital for healthy eating behavior. Patients with binge eating disorder (BED) suffer under recurrent binge eating episodes accompanied by subjective loss of control that results, among other factors, from increased impulsivity.MethodsIn the current study, we investigated the frontal network using functional near-infrared spectroscopy (fNIRS) during a food specific go/nogo task to assess response inhibition in 24 patients with BED (BMI range 22.6-59.7 kg/m2) compared to 12 healthy controls (HC) (BMI range 20.9-27 kg/m2). Patients with BED were invited to undergo fNIRS measurements before an impulsivity-focused cognitive behavioral group treatment, directly after this treatment and 3 months afterwards. As this was a planned subgroup analysis of the randomized controlled IMPULS trial, patients with BED were randomized either to the treatment group (n = 14) or to a control group (n = 10). The treatment group received 8 weekly sessions of the IMPULS treatment.ResultsWe found a significant response inhibition effect (nogo minus go), in terms of an increased oxygenated hemoglobin response in the bilateral prefrontal cortex in both groups. The greatest response was observed when participants were instructed to go for healthy and withhold their response to unhealthy high caloric food cues. The healthy nogo condition failed to show a significant prefrontal inhibitory response, which was probably related to the task design, as the condition was considered more demanding. BED patients, especially those with higher trait impulsivity, showed a weaker activation of the prefrontal cortex during response inhibition, predominantly in the right hemisphere. Interestingly, three months after the treatment, patients of the treatment group increased their right prefrontal cortex activity during response inhibition. Likewise, increased prefrontal cortex activation correlated with decreased trait impulsivity after treatment.ConclusionsOur results suggest that patients with BED have limited resources to activate the prefrontal cortex when asked to inhibit a reaction onto food-specific stimuli. However, this effect could be partly driven by differences in BMI between the HC and BED group. Cognitive-behavioral therapy targeting impulsive eating behavior may improve prefrontal cortex recruitment during response inhibition.

Dataset Information

Lateral prefrontal model-based signatures are reduced in healthy individuals with high trait impulsivity.

Publications

Lateral prefrontal model-based signatures are reduced in healthy individuals with high trait impulsivity.

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