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The role of the basal ganglia in habit formation

Key Points

  • The basal ganglia are a set of subcortical nuclei in the cerebrum that are involved in the integration and selection of voluntary behaviour. The striatum, the major input station of the basal ganglia, has a key role in instrumental behaviour — learned behaviour that is modified by its consequences.

  • Reward-guided instrumental behaviours usually start as goal-directed actions that are controlled by the anticipation of the outcome, but under certain conditions these behaviours can become stimulus-driven habits, which are not controlled by outcome expectancy.

  • Habits can be operationally defined as instrumental behaviour that is impervious to changes in the value of the outcome and in the causal contingency between action and outcome. Behavioural assays that directly manipulate these variables have become indispensable in the analysis of habit formation.

  • The dorsal striatum is traditionally viewed as a substrate for stimulus–response habit learning, but more recent evidence indicates that this view requires modification. A more detailed analysis using modern behavioural assays reveals considerable functional heterogeneity in the dorsal striatum.

  • The dorsolateral, or sensorimotor, striatum (DLS) and the dorsomedial, or associative, striatum (DMS) differ in their anatomical connectivity, distribution of key receptors, and rules of synaptic plasticity. They can also be doubly dissociated functionally, with the DLS being crucial for stimulus-driven habits and the DMS being crucial for goal-directed actions.

  • The DMS and DLS belong to distinct cortico-basal ganglia networks, mediating actions and habits, respectively. The process of habit formation in instrumental learning finds its neural correlate in a shift of control from the associative to the sensorimotor cortico-basal ganglia network.

Abstract

Many organisms, especially humans, are characterized by their capacity for intentional, goal-directed actions. However, similar behaviours often proceed automatically, as habitual responses to antecedent stimuli. How are goal-directed actions transformed into habitual responses? Recent work combining modern behavioural assays and neurobiological analysis of the basal ganglia has begun to yield insights into the neural basis of habit formation.

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Figure 1: A schematic of the main connections of the basal ganglia.
Figure 2: Simple maze tasks for measuring habits and actions.
Figure 3: Cortico-basal ganglia networks as the fundamental motifs of cerebral organization.
Figure 4: Schematic illustration of hypothetical mechanisms for the detection of instrumental contingency in appetitive instrumental learning.

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Acknowledgements

H.H.Y. was supported by the Intramural Research Program at the National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health. B.J.K. was supported by a National Science Foundation grant. We would like to thank B. Balleine, R. Costa, N. Daw, T. Dickinson and S. Ostlund for helpful discussion.

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Glossary

Extinction

Operationally, the withholding of reinforcement after previous reinforcement.

Temporal-difference algorithm

A reinforcement learning method that is driven by the difference between temporally successive predictions, rather than by the difference between predicted and actual outcomes.

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A stochastic control process with the Markov property: future states are conditionally independent of past states and depend only on the current state.

Stereotypy

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Striosome

A patch-like compartment in the striatum that is characterized by low acetylcholinesterase staining and other chemical markers.

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Yin, H., Knowlton, B. The role of the basal ganglia in habit formation. Nat Rev Neurosci 7, 464–476 (2006). https://doi.org/10.1038/nrn1919

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