Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients

Z Sjoerds,B W J H Penninx,W Van Den Brink,T W Robbins,A T F Beekman,D J Veltman,S De Wit

doi:10.1038/tp.2013.107

Abstract

Substance dependence is characterized by compulsive drug-taking despite negative consequences. Animal research suggests an underlying imbalance between goal-directed and habitual action control with chronic drug use. However, this imbalance, and its associated neurophysiological mechanisms, has not yet been experimentally investigated in human drug abusers. The aim of the present study therefore was to assess the balance between goal-directed and habit-based learning and its neural correlates in abstinent alcohol-dependent (AD) patients. A total of 31 AD patients and 19 age, gender and education matched healthy controls (HC) underwent functional magnetic resonance imaging (fMRI) during completion of an instrumental learning task designed to study the balance between goal-directed and habit learning. Task performance and task-related blood oxygen level-dependent activations in the brain were compared between AD patients and healthy matched controls. Findings were additionally associated with duration and severity of alcohol dependence. The results of this study provide evidence for an overreliance on stimulus-response habit learning in AD compared with HC, which was accompanied by decreased engagement of brain areas implicated in goal-directed action (ventromedial prefrontal cortex and anterior putamen) and increased recruitment of brain areas implicated in habit learning (posterior putamen) in AD patients. In conclusion, this is the first human study to provide experimental evidence for a disturbed balance between goal-directed and habitual control by use of an instrumental learning task, and to directly implicate cortical dysfunction to overreliance on inflexible habits in AD patients.

Highlights

Animal research suggests that this shift from casual to compulsive drug use is based on increased habit formation at the expense of flexible, goal-directed action control.[7,8,9,10]
All imaging analyses were performed whole-brain, but we focused on areas we found in the analyses that are known to be involved in goaldirected and habit learning:[18,19,20,23,24,47] ventromedial prefrontal cortex (VMPFC), anterior putamen and caudate head for goal-directed learning, and posterior putamen and caudate tail/body for habit learning
The alcohol dependence (AD) group contained smokers, whereas the healthy controls (HC) group did not, and scored higher on alcohol use as well as depression and anxiety severity compared to the HCs

Summary

Introduction

Substance use disorders like alcohol dependence (AD) are regarded to be chronic, relapsing brain diseases.[1,2,3] initial drug intake is associated with positive reinforcement and impulsive actions, chronic drug use is characterized by compulsive drug-taking behavior despite negative consequences.[4,5,6] Animal research suggests that this shift from casual to compulsive drug use is based on increased habit formation at the expense of flexible, goal-directed action control.[7,8,9,10] Yet, little is known about the mechanisms underlying this process in human drug abuse, and experimental evidence regarding the neuro-adaptations that develop during chronic alcohol use in humans is lacking.According to dual-systems accounts, two dissociable learning processes can be identified in instrumental behavior.[11,12] On one hand, goal-directed actions are performed in order to achieve desirable goals (positive reinforcement) or to avoid undesirable outcomes (negative reinforcement). We examined the balance between goal-directed and habit learning, and its neural correlates, in abstinent AD patients and healthy controls (HC) during functional magnetic resonance imaging current substance use disorders (other than alcohol for the AD group and smoking).

Results

Conclusion