Review

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

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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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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.

Author information

Affiliations

  1. Neuroscience Research Unit, Department of Psychology, University of Sheffield, S10 2TP, UK.

    • Peter Redgrave
  2. Department of Physiology, Medical School, University of La Laguna, Tenerife, 38201, Spain.

    • Manuel Rodriguez
  3. Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Instituto Carlos III, Ministerio de Investigacion y Ciencias, 28038, Spain.

    • Manuel Rodriguez
    • , Maria C. Rodriguez-Oroz
    •  & Jose A. Obeso
  4. Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30329, USA.

    • Yoland Smith
  5. Department of Neurology, Emory University School of Medicine, Atlanta, Georgia 30322, USA.

    • Yoland Smith
    •  & Mahlon R. DeLong
  6. Movement Disorders Group, Neurosciences Division, CIMA and Department of Neurology and Neurosurgery, Clínica Universidad de Navarra, Pamplona, 31008, Spain.

    • Maria C. Rodriguez-Oroz
    •  & Jose A. Obeso
  7. Centre de NeuroImagerie de Recherche (CENIR), Institut du Cerveau et de la Moelle épinière (ICM), Universite Pierre et Marie Curie, Inserm U975, CNRS 7225, Groupe Hospitalier Pitié-Salpêtrière, 75013, Paris, France.

    • Stephane Lehericy
  8. Hebrew University, Hadassah Medical School, Jerusalem 91120, Israel.

    • Hagai Bergman
  9. Institut du Cerveau et de la Moelle épinière (ICM), 75013, Paris, France.

    • Yves Agid

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Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Peter Redgrave or Jose A. Obeso.

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'.