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Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease

Key Points

  • The basal ganglia are one of the fundamental processing units of the mammalian brain. Progressive degeneration of one of their major components, the ascending dopamine projection to the striatum, is a central pathological feature of Parkinson's disease.

  • Imaging and post-mortem investigations reveal that degeneration of the dopamine projection is uneven in most cases, with input to caudolateral sectors of the putamen most severely affected.

  • In the animal learning literature an important distinction has been forged between goal-directed and habitual control of behaviour. When behaviour is goal-directed, action selection is determined by the relative utility of predicted outcomes, whereas habits are under stimulus control and largely independent of outcome value.

  • A seminal series of investigations in rodents by Balleine and colleagues established that the dorsomedial associative territories of the striatum are crucial for goal-directed control, whereas laterally located sensorimotor territories are essential for habits. Formal behavioural tests (for example, outcome devaluation) were used to determine whether an observed behaviour (for example, pressing a lever) was under goal-directed or habitual control.

  • Recent neuroimaging studies using the same formal tests suggest that a similar spatial segregation of goal-directed and habitual control is present within the human striatum. As the loss of dopamine in Parkinson's disease is predominantly from the caudolateral sensorimotor territories, we would expect patients to experience major deficits in their production of habits.

  • Because the same behavioural output can be directed by processing in spatially segregated regions of the basal ganglia, it must be assumed that the efferent projections of goal-directed and habitual control circuits must at some point converge on the 'final common motor path'.

  • Given that the loss of dopamine in the basal ganglia is associated with enhanced oscillatory and inhibitory outputs, we suggest that for goal-directed control to be expressed, the distorting inhibitory signals from the habit system must be overcome at the point where the goal-directed and habitual control circuits converge.

  • We conclude by reviewing evidence suggesting that many of the behavioural difficulties experienced by patients with Parkinson's disease can be interpreted in terms of an impaired automatic control of normal habits, coupled with distorting inhibitory influences imposed on the expression of residual goal-directed behaviours.

  • In the light of this analysis, future work will need to establish how far the reported cognitive deficits in Parkinson's disease are due to the primary disease state (additional loss of dopamine from goal-directed circuits) or are a result of goal-directed control being overwhelmed by the absence of automatic control routines that are normally provided by the stimulus–response habit systems.

Abstract

Progressive loss of the ascending dopaminergic projection in the basal ganglia is a fundamental pathological feature of Parkinson's disease. Studies in animals and humans have identified spatially segregated functional territories in the basal ganglia for the control of goal-directed and habitual actions. In patients with Parkinson's disease the loss of dopamine is predominantly in the posterior putamen, a region of the basal ganglia associated with the control of habitual behaviour. These patients may therefore be forced into a progressive reliance on the goal-directed mode of action control that is mediated by comparatively preserved processing in the rostromedial striatum. Thus, many of their behavioural difficulties may reflect a loss of normal automatic control owing to distorting output signals from habitual control circuits, which impede the expression of goal-directed action.

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Figure 1: Organization of intrinsic connections within the basal ganglia.
Figure 2: Corticobasal ganglia–cortical loops in animals and humans.
Figure 3: Striatal determinants of goal-directed and habitual action in rodents and humans.
Figure 4: Striatal dopamine innervation assessed by 18fluorodopa positron emission tomography (PET).
Figure 5: Functional and dysfunctional loops through the basal ganglia in the parkinsonian state.

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Acknowledgements

This article arose as a result of a meeting ('From movement to behaviour and emotions: role of the basal ganglia') held in December 2008 at the Centro Internacional de Restauracion Neurologica (CIREN) in Havana, Cuba. The meeting was organized by the CIREN and the Neuroscience Department, CIMA, University of Navarra, Pamplona, Spain, and sponsored by private donations. Authors are grateful to J. Alvarez, President of CIREN, and D. Frontera and family for their support and contribution to the project's success. P.R. was supported by a European Framework 7 grant and the Wellcome Trust, and J.A.O. by the University of Navarra–Union Temporal de Empresas (UTE) agreement during the preparation of this article. We thank B. Balleine for providing us with a high resolution copy of figure 3, and C. Juri and J. Arbizu for the PET images in figure 4.

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Glossary

Basal ganglia

One of the fundamental processing units of the vertebrate brain. In mammals they comprise the striatum, globus pallidus, substantia nigra and subthalamic nucleus.

Striatum

The principal input nucleus of the basal ganglia consisting of the caudate nucleus and putamen.

Parkinsonian state

A state characterized by akinesia, bradykinesia and tremor associated in the initial stages with a differential loss of dopamine from the sensorimotor territories of the striatum.

Dyskinetic state

A state characterized by involuntary, repetitive body movements.

Hemiballismus

A movement disorder that is characterized by large-amplitude involuntary flinging motions of the extremities.

Instrumental learning

Learning in which a reinforcing outcome is contingent on the performance (or withholding) of a particular behaviour. Thus, the subject's response is 'instrumental' in producing an outcome (typically a food reward).

Associative learning

Any learning process in which a new response becomes associated with a particular stimulus. In animal behaviour it generally denotes learning that occurs through classical and instrumental conditioning.

Fixed ratio schedules

(Often abbreviated to FR schedules.) Situations in which there is a fixed relationship between responses and outcomes. For example, in an FR3 schedule, every third response is reinforced.

Interval schedules

Reinforcement is delivered with the first response following a fixed or variable interval, making the association between response and outcome much weaker.

Set shifting

The ability to modify ongoing behaviour in response to changing goals or environmental experiences.

6-hydroxydopamine lesion model of Parkinson's disease

A neurotoxin that, when administered to the substantia nigra of rodents, causes degeneration of the ascending nigrostriatal dopaminergic pathway, thereby mimicking the loss of dopaminergic innervation in Parkinson's disease.

Oscillations

(Referring here to oscillations in Parkinson's disease.) Resting tremor that is thought to be related to the increased levels of synchronous neuronal activity observed within the basal ganglia of patients with Parkinson's disease and in animal models of the disease.

Abulia

A condition characterized by a reduction in goal-directed verbal, motor, cognitive and emotional behaviours and that is associated with focal lesions of the basal ganglia.

Poverty of thought

A form of 'psychic akinesia' in which patients are generally apathetic and exhibit a profound lack of 'will'.

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Redgrave, P., Rodriguez, M., Smith, Y. et al. Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat Rev Neurosci 11, 760–772 (2010). https://doi.org/10.1038/nrn2915

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