Elsevier

Alcohol

Volume 49, Issue 8, December 2015, Pages 817-824
Alcohol

Corticostriatal circuitry and habitual ethanol seeking

https://doi.org/10.1016/j.alcohol.2015.03.003Get rights and content

Highlights

  • Alcohol use disorders involve inflexible alcohol seeking.

  • Models of habitual behavior may be used to investigate uncontrolled alcohol seeking.

  • The expression of habitual behavior is mediated in part by corticostriatal circuits.

  • Alcohol exposure disrupts these circuits, likelyimpairing behavioral flexibility.

  • A greater understanding of alcohol effects on these circuits may point to novel treatments.

Abstract

The development of alcohol-use disorders is thought to involve a transition from casual alcohol use to uncontrolled alcohol-seeking behavior. This review will highlight evidence suggesting that the shift toward inflexible alcohol seeking that occurs across the development of addiction consists, in part, of a progression from goal-directed to habitual behaviors. This shift in “response strategy” is thought to be largely regulated by corticostriatal network activity. Indeed, specific neuroanatomical substrates within the prefrontal cortex and the striatum have been identified as playing opposing roles in the expression of actions and habits. A majority of the research on the neurobiology of habitual behavior has focused on non-drug reward seeking. Here, we will highlight recent research identifying corticostriatal structures that regulate the expression of habitual alcohol seeking and a comparison will be made when possible to findings for non-drug rewards.

Introduction

Identification of the neurobiological substrates of habitual ethanol seeking may help to guide the development of novel therapeutic strategies that can enable restoration of behavioral control. While reducing ethanol-seeking habits is not expected to be a stand-alone cure for addiction, or a solution for all individuals with alcohol-use disorders, the ability to restore cognitive control over ethanol-seeking behaviors may enable traditional therapeutic strategies. Despite the applicability of this model to addictive behavior (Everitt, 2014, Kalivas, 2008), a preponderance of the research into the neuroscience of habitual behavior has been performed with models of non-drug reward seeking (e.g., Yin & Knowlton, 2006), rather than ethanol. While it can be argued that the structures mediating non-drug habits regulate the development of habitual behavior in general, recent work suggests that alcohol reinforcers may differentially engage the neurocircuits that control behavioral flexibility (Barker et al., 2014, Corbit et al., 2012, Mangieri et al., 2012, Shillinglaw et al., 2014). In this review, we will focus on the novel application and extension of these findings to the development of habitual ethanol-seeking behavior that, in part, characterizes alcohol-use disorders. We will provide a framework for the role of habitual processes in ethanol-seeking behavior and summarize findings presented at the 2014 Alcoholism and Stress Meeting in Volterra, Italy with the intention to highlight novel observations on the role for corticostriatal circuits in the regulation of ethanol-seeking behavior (for a more in-depth review of the neuroanatomy of habitual processes in ethanol seeking, see Barker and Taylor, 2014, O'Tousa and Grahame, 2014).

Section snippets

Modeling conditioned behavior in alcohol-use disorders

In recent years, there has been a burgeoning interest in understanding drug seeking that is not mediated by the immediate rewarding properties of drugs of abuse. Work in both animals and humans has suggested drugs of abuse, including alcohol, are sought not only for their positive rewarding properties, but also out of habit (Adams, 1982, Dickinson et al., 2002, Robbins and Everitt, 1999). In other words, while drugs of abuse are initially sought for their rewarding properties, over time and

Regulation of reward seeking within the striatum

A significant literature has identified striatal subregions as critical regulators of reward-seeking behavior. While the ventral striatum is thought to be largely involved with cued outcome-mediated behaviors, the more dorsal aspects of the striatum appear to have distinct contributions to goal-directed and habitual reward-seeking behavior. The nucleus accumbens (NAc) can be subdivided into two primary subregions – the NAc shell and the core – with distinct network connectivity with the

Corticostriatal circuits and response-strategy selection

In addition to the unique contributions of striatal subregions to the expression of goal-directed actions and habitual behaviors, cortical structures that project to the striatum are critical in the regulation of reward-seeking behavior. A majority of work pointing to cortical control of habitual behavior has implicated structures within the medial PFC, including the infralimbic and prelimbic subregions. The prelimbic PFC sends glutamatergic projections to the NAc core and DMS, as well as

Ethanol effects on corticostriatal function and the development of treatment strategies

Recent research has identified a number of conditions under which ethanol exposure can alter behavioral flexibility. Habit models have shown that ethanol-seeking habits may develop more rapidly than those for non-drug rewards in animals that are self-administering ethanol (Corbit et al., 2012, Dickinson et al., 2002). Importantly, while animals self-administer pharmacologically relevant doses in recent studies of habitual ethanol seeking (0.4–2.0 g ethanol per kg body weight, varying by study),

Acknowledgments

This research was supported by National Institutes of Health Grants AA007474 and AA023141 (JMB), AA010761 and AA010983 (LJC), AA11852 (RAG), AA018008 (DLR), Australian National Health and Medical Research Council 1051037 (LHC), DICBR NIAAA (CMG) and NIAAA Conference Grant AA071581. The authors would like to acknowledge the contributions of Patricia Janak, Jane Taylor, and Rui Costa to the work presented in these proceedings.

References (99)

  • A.C. Roberts

    Primate orbitofrontal cortex and adaptive behaviour

    Trends in Cognitive Sciences

    (2006)
  • H.H. Samson et al.

    Devaluation of ethanol reinforcement

    Alcohol

    (2004)
  • N. Schmitzer-Torbert et al.

    Post-training cocaine administration facilitates habit learning and requires the infralimbic cortex and dorsolateral striatum

    Neurobiology of Learning and Memory

    (2015)
  • J.E. Shillinglaw et al.

    Assessing behavioral control across reinforcer solutions on a fixed-ratio schedule of reinforcement in rats

    Alcohol

    (2014)
  • T.M. Tzschentke

    Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues

    Progress in Neurobiology

    (1998)
  • P. Voorn et al.

    Putting a spin on the dorsal-ventral divide of the striatum

    Trends in Neurosciences

    (2004)
  • H.H. Yin et al.

    Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning

    Behavioural Brain Research

    (2006)
  • C.D. Adams

    Variations in the sensitivity of instrumental responding to reinforcer devaluation

    The Quarterly Journal of Experimental Psychology, Section B: Comparative and Physiological Psychology

    (1982)
  • C. Adams et al.

    Actions and habits: variations in associative representations during instrumental learning

  • B.W. Balleine et al.

    Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action

    Neuropsychopharmacology

    (2010)
  • J.M. Barker et al.

    A unifying model of the role of the infralimbic cortex in extinction and habits

    Learning & Memory

    (2014)
  • J.M. Barker et al.

    Brain-derived neurotrophic factor and addiction: pathological versus therapeutic effects on drug seeking

    Brain Research

    (2014)
  • J.M. Barker et al.

    Low prefrontal PSA-NCAM confers risk for alcoholism-related behavior

    Nature Neuroscience

    (2012)
  • J.M. Barker et al.

    Bidirectional modulation of infralimbic dopamine D1 and D2 receptor activity regulates flexible reward seeking

    Frontiers in Neuroscience

    (2013)
  • J.M. Barker et al.

    Epigenetic and pharmacological regulation of 5HT3 receptors controls compulsive ethanol seeking in mice

    The European Journal of Neuroscience

    (2014)
  • R. Bock et al.

    Strengthening the accumbal indirect pathway promotes resilience to compulsive cocaine use

    Nature Neuroscience

    (2013)
  • N. Chaudhri et al.

    Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking

    Neuropsychopharmacology

    (2010)
  • R.M. Colwill et al.

    Instrumental responding remains sensitive to reinforcer devaluation after extensive training

    Journal of Experimental Psychology: Animal Behavior Processes

    (1985)
  • L.H. Corbit et al.

    Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer

    The Journal of Neuroscience

    (2005)
  • L.H. Corbit et al.

    The general and outcome-specific forms of Pavlovian-instrumental transfer are differentially mediated by the nucleus accumbens core and shell

    The Journal of Neuroscience

    (2011)
  • L.H. Corbit et al.

    Ethanol-associated cues produce general pavlovian-instrumental transfer

    Alcoholism: Clinical and Experimental Research

    (2007)
  • L.H. Corbit et al.

    Posterior dorsomedial striatum is critical for both selective instrumental and Pavlovian reward learning

    The European Journal of Neuroscience

    (2010)
  • L.H. Corbit et al.

    General and outcome-specific forms of Pavlovian-instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area

    The European Journal of Neuroscience

    (2007)
  • L.H. Corbit et al.

    The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell

    The Journal of Neuroscience

    (2001)
  • L.H. Corbit et al.

    Habitual responding for alcohol depends upon both AMPA and D2 receptor signaling in the dorsolateral striatum

    Frontiers in Behavioral Neuroscience

    (2014)
  • L. DePoy et al.

    Chronic alcohol produces neuroadaptations to prime dorsal striatal learning

    Proceedings of the National Academy of Sciences of the United States of America

    (2013)
  • L. Depoy et al.

    Chronic alcohol alters rewarded behaviors and striatal plasticity

    Addiction Biology

    (2015)
  • A. Dickinson

    Actions and habits: the development of behavioural autonomy

    Philosophical Transactions of the Royal Society B: Biological Sciences

    (1985)
  • A. Dickinson et al.

    Alcohol seeking by rats: action or habit?

    The Quarterly Journal of Experimental Psychology. Section B, Comparative and Physiological Psychology

    (2002)
  • B.J. Everitt

    Neural and psychological mechanisms underlying compulsive drug seeking habits and drug memories – indications for novel treatments of addiction

    The European Journal of Neuroscience

    (2014)
  • R.R. Fanelli et al.

    Dorsomedial and dorsolateral striatum exhibit distinct phasic neuronal activity during alcohol self-administration in rats

    The European Journal of Neuroscience

    (2013)
  • A. Faure et al.

    Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation

    The Journal of Neuroscience

    (2005)
  • S.V. Glasner et al.

    The role of Pavlovian cues in alcohol seeking in dependent and nondependent rats

    Journal of Studies on Alcohol

    (2005)
  • S.L. Gourley et al.

    Dissociable regulation of instrumental action within mouse prefrontal cortex

    The European Journal of Neuroscience

    (2010)
  • S.L. Gourley et al.

    The orbitofrontal cortex regulates outcome-based decision-making via the lateral striatum

    The European Journal of Neuroscience

    (2013)
  • C.M. Gremel et al.

    Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions

    Nature Communications

    (2013)
  • C.M. Gremel et al.

    Roles of the nucleus accumbens and amygdala in the acquisition and expression of ethanol-conditioned behavior in mice

    The Journal of Neuroscience

    (2008)
  • W.C. Griffin et al.

    Increased extracellular glutamate in the nucleus accumbens promotes excessive ethanol drinking in ethanol dependent mice

    Neuropsychopharmacology

    (2013)
  • R.A. Hay et al.

    Specific and nonspecific effects of naltrexone on goal-directed and habitual models of alcohol seeking and drinking

    Alcoholism: Clinical and Experimental Research

    (2013)
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