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  • Review Article
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A fronto–striato–subthalamic–pallidal network for goal-directed and habitual inhibition

Nature Reviews Neuroscience volume 16, pages 719–732 (2015)Cite this article

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Key Points

  • We propose that the fronto–striatal circuits play a part not only in goal-directed and habitual action but also in goal-directed and habitual (automatic) inhibitory control.

  • We propose that the fronto–striatal network mediates goal-directed and habitual inhibition across motor and non-motor domains.

  • We propose that some of the symptoms of Parkinson's disease, Tourette syndrome and obsessive–compulsive disorder represent an imbalance between goal-directed and habitual action and inhibition.

  • We review evidence from animal studies, functional imaging studies, investigations in Parkinson's disease, Tourette syndrome and obsessive–compulsive disorder and the surgical treatment of these disorders, in support of our proposal that the fronto–striatal network mediates goal-directed and habitual inhibition.

  • We highlight key questions that remain to be addressed in relation to the role of the fronto–striatal network in goal-directed and habitual inhibition.

Abstract

Classically, the basal ganglia have been considered to have a role in producing habitual and goal-directed behaviours. In this article, we review recent evidence that expands this role, indicating that the basal ganglia are also involved in neural and behavioural inhibition in the motor and non-motor domains. We then distinguish between goal-directed and habitual (also known as automatic) inhibition mediated by fronto–striato–subthalamic–pallido–thalamo–cortical networks. We also suggest that imbalance between goal-directed and habitual action and inhibition contributes to some manifestations of Parkinson's disease, Tourette syndrome and obsessive–compulsive disorder. Finally, we propose that basal ganglia surgery improves these disorders by restoring a functional balance between facilitation and inhibition.

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Figure 1: The main functional subdivisions in the sensorimotor, associative and limbic cortico–striatal circuits.
Figure 2: The hyperdirect, direct and indirect pathways and neural inhibition in the cortico–basal ganglia circuits.
Figure 3: The fronto–basal ganglia pathways mediating proactive and reactive inhibitory control.

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Authors and Affiliations

  1. Sobell Department of Motor Neuroscience & Movement Disorders, University College London Institute of Neurology and The National Hospital for Neurology and Neurosurgery, London, WC1N 3BG, UK

    Marjan Jahanshahi & John C. Rothwell

  2. Centro Integral de Neurociencias AC (CINAC), HM Puerta del Sur, Hospitales de Madrid Mostoles, Madrid, 28938, Spain

    Ignacio Obeso & José A. Obeso

  3. CEU San Pablo University, Campus de Moncloa, Calle Julián Romea, 18, Madrid, 28003, Spain

    Ignacio Obeso & José A. Obeso

  4. Centro de Investigación Biomédica en Red, Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain

    Ignacio Obeso & José A. Obeso

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Glossary

Habit

A learned behaviour that is performed regularly and automatically without much attention being required.

Levodopa-induced dyskinesias

(LIDs). Involuntary movements induced by levodopa medication.

Reversal learning

Learning to inhibit responses to a stimulus that is no longer rewarded and instead to respond to an alternative, new stimulus.

Cognitive reappraisal

'Reframing' how one thinks about a situation, which can be important for emotion regulation.

Prosody

The rhythm, stress and intonation of speech.

Hobbyism

Excessive devotion to hobbies.

Punding

Complex, prolonged, repetitive, purposeless and stereotyped behaviour.

Dopamine-dysregulation syndrome

An excessive and addiction-like overuse of dopaminergic medication.

Logorrhoea

A tendency towards excessive and often incoherent talkativeness or wordiness and repetitiveness of speech.

Simon effect

The finding that, in a task in which stimulus location is irrelevant to task performance, reaction times are usually faster and responses are more accurate when a stimulus occurs in the same relative location as the response than when the stimulus and response positions are incompatible.

Probabilistic decision making

Making decisions based on stimuli that indicate different probabilities of obtaining a reward.

Decision conflict

Difficulty in making decisions and selecting one option over another, for example, when the expected probability of the reward associated with two stimuli is equally high.

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Jahanshahi, M., Obeso, I., Rothwell, J. et al. A fronto–striato–subthalamic–pallidal network for goal-directed and habitual inhibition. Nat Rev Neurosci 16, 719–732 (2015). https://doi.org/10.1038/nrn4038

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