Review
The integrative function of the basal ganglia in instrumental conditioning

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Abstract

Recent research in instrumental conditioning has focused on the striatum, particularly the role of the dorsal striatum in the learning processes that contribute to instrumental performance in rats. This research has found evidence of what appear to be parallel, functionally and anatomically distinct circuits involving dorsomedial striatum (DMS) and dorsolateral striatum (DLS) that contribute to two independent instrumental learning processes. Evidence suggests that the formation of the critical action–outcome associations mediating goal-directed action are localized to the dorsomedial striatum, whereas the sensorimotor connections that control the performance of habitual actions are localized to the dorsolateral striatum. In addition to the dorsal striatum, these learning processes appear to engage distinct cortico-striatal networks and to be embedded in a complex of converging and partially segregated loops that constitute the cortico-striatal thalamo-cortical feedback circuit. As the entry point for the basal ganglia, cortical circuits involving the dorsal striatum are clearly in a position to control a variety of motor functions but, as recent studies of various neurodegenerative disorders have made clear, they are also involved in a number of cognitive and executive functions including action selection, planning, and decision-making.

Section snippets

Cognition, behavioral control and Pavlovian conditioning

Paradoxically, although the cognitive control of behavior has been of increasing interest to neuroscientists, research in this area has focused predominantly on predictive learning in Pavlovian conditioning paradigms such as fear conditioning and eye-blink conditioning. There is, however, no necessary relationship between cognition and the performance of the Pavlovian conditioned response (CR). Indeed, although it is not generally recognized, at an adaptive level a cognitive mechanism is of

Habitual action

Input to the striatum from sensorimotor cortex, particularly primary motor and somatosensory cortices (cf. [83], [84]), appears to be involved in what is commonly thought to be a completely different form of performance process involving the control of actions by antecedent stimuli through a traditional S–R/reinforcement associative mechanism. In recent years this process has been argued to form the core of a distinct functional capacity involving the formation of habitual actions. Habits are

Competition or cooperation?

Together, the findings from the experimental investigations of the dorsal striatum described above have identified two distinct functional systems within adjacent regions of dorsal striatum: specifically, a circuit mediating goal-directed learning and involving the dorsomedial striatum and a circuit mediating habit or procedural learning and involving the dorsolateral striatum. Furthermore, at least at the level of the striatum these functions appear to be independent; damage to dorsolateral

Summary and conclusion

Whatever the neural bases of the interaction between goal-directed and habitual processes turns out to be, recent data suggest that the basal ganglia are able to maintain these functions in parallel and allow, under some conditions, one or other process either independent control or, under other conditions, both processes to exert cooperative control over the performance of instrumental actions. It is important to note that, in suggesting that two distinct learning processes are concurrently

References (144)

  • Y. Niv et al.

    A normative perspective on motivation

    Trends Cogn Sci

    (2006)
  • T. Winograd

    Frame representations and the declarative-procedural controversy

  • M. Laubach

    Who's on first? What's on second? The time course of learning in corticostriatal systems

    Trends Neurosci

    (2005)
  • D.C. Ding et al.

    Differences in the laminar origin of projections from the medial prefrontal cortex to the nucleus accumbens shell and core regions in the rat

    Brain Res

    (2001)
  • A.E. Kelley et al.

    The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods

    Neuroscience

    (1982)
  • T.W. Robbins et al.

    Limbic-striatal memory systems and drug addiction

    Neurobiol Learn Mem

    (2002)
  • E.W. Holman

    Some conditions for the dissociation of consummatory and instrumental behavior in rats

    Learn Motiv

    (1975)
  • H.H. Yin et al.

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

    Behav Brain Res

    (2006)
  • R.M. Costa et al.

    Differential corticostriatal plasticity during fast and slow motor skill learning in mice

    Curr Biol

    (2004)
  • R.M. Costa et al.

    Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction

    Neuron

    (2006)
  • E.L. Thorndike

    Animal intelligence: experimental studies

    (1911)
  • C.L. Hull

    Principles of behavior

    (1943)
  • E.R. Guthrie

    The psychology of learning

    (1935)
  • K.W. Spence

    Behavior theory and conditioning

    (1956)
  • A. Dickinson et al.

    Actions and responses: the dual psychology of behaviour

  • A. Dickinson et al.

    Motivational control of goal-directed action

    Anim Learn Behav

    (1994)
  • A. Dickinson et al.

    The role of learning in motivation

  • B.W. Balleine et al.

    The role of incentive learning in instrumental outcome revaluation by specific satiety

    Anim Learn Behav

    (1998)
  • B.W. Balleine

    Incentive processes in instrumental conditioning

  • B.W. Balleine et al.

    Still at the choicepoint: action selection and initiation in instrumental conditioning

    Ann N Y Acad Sci

    (2007)
  • B.W. Balleine et al.

    Multiple forms of value learning and the function of dopamine

  • H.H. Yin et al.

    Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks

    Eur J Neurosci

    (2008)
  • S.B. Ostlund et al.

    Orbitofrontal cortex mediates outcome encoding in Pavlovian but not instrumental learning

    J Neurosci

    (2007)
  • J. Konorski et al.

    On two types of conditioned reflex

    J Gen Psychol

    (1937)
  • F.D. Sheffield

    Relation between classical and instrumental conditioning

  • P.C. Holland

    Differential effects of omission contingencies on various components of Pavlovian appetitive conditioned responding in rats

    J Exp Psychol Anim Behav Process

    (1979)
  • W.A. Hershberger

    An approach through the looking-glass

    Anim Learn Behav

    (1986)
  • A. Dickinson

    Expectancy theory in animal conditioning

  • C.D. Frith et al.

    Willed action and the prefrontal cortex in man: a study with PET

    Proc R Soc Lond

    (1991)
  • R.T. Knight et al.

    Role of human prefrontal cortex in attention control

    Adv Neurol

    (1995)
  • M.D. Lezak

    Neuropsychological assessment

    (1995)
  • C.-C. Chu et al.

    The autonomic-related cortex: pathology in Alzheimer's disease

    Cereb Cortex

    (1997)
  • J.L. Rapoport et al.

    The new biology of obsessive-compulsive disorder: implications for evolutionary psychology

    Perspect Biol Med

    (1998)
  • D. Robinson et al.

    Reduced caudate nucleus volume in obsessive-compulsive disorder

    Arch Gen Psychiatry

    (1995)
  • M.H. Bloch et al.

    Caudate volumes in childhood predict symptom severity in adults with Tourette syndrome

    Neurology

    (2005)
  • A. Hodges et al.

    Regional and cellular gene expression changes in human Huntington's disease brain

    Hum Mol Genet

    (2006)
  • A.R. Damasio

    The somatic marker hypothesis and the possible functions of the prefrontal cortex

    Philos Trans R Soc Lond B Biol Sci

    (1996)
  • F. Dretske

    Explaining behavior: reasons in a world of causes

    (1988)
  • M.E. Bratman

    Intention, plans and practical reason

    (1987)
  • M. Frese et al.

    Goal directed behavior: the concept of action in psychology

    (1985)
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    The preparation of this article and the research it describes were supported by grants from the NIMH #56446 and NICHD #59257.

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