Volume 31, Issue 8 p. 1146-1154
Research Article

The globus pallidus pars interna in goal-oriented and routine behaviors: Resolving a long-standing paradox

Camille Piron PhD

Camille Piron PhD

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

CNRS, French-Israeli Neuroscience Lab, Bordeaux, France

Camille Piron and Daisuke Kase contributed equally to this work.

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Daisuke Kase PhD

Daisuke Kase PhD

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

CNRS, French-Israeli Neuroscience Lab, Bordeaux, France

Camille Piron and Daisuke Kase contributed equally to this work.

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Meropi Topalidou BsC

Meropi Topalidou BsC

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

INRIA, Bordeaux Sud-Ouest, Talence, France

University of Bordeaux, UMR 5800, LABRI, IPB, Talence, France

CNRS, UMR 5800, LABRI, IPB, Talence, France

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Michel Goillandeau

Michel Goillandeau

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

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Hugues Orignac

Hugues Orignac

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

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Tho-Haï N'Guyen

Tho-Haï N'Guyen

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

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Nicolas Rougier PhD

Nicolas Rougier PhD

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

INRIA, Bordeaux Sud-Ouest, Talence, France

University of Bordeaux, UMR 5800, LABRI, IPB, Talence, France

CNRS, UMR 5800, LABRI, IPB, Talence, France

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Thomas Boraud MD, PhD

Corresponding Author

Thomas Boraud MD, PhD

University of Bordeaux, UMR 5293, IMN, Bordeaux, France

CNRS, UMR 5293, IMN, Bordeaux, France

CNRS, French-Israeli Neuroscience Lab, Bordeaux, France

CHU de Bordeaux, IMN Clinique, Bordeaux, France

Correspondence to: Thomas Boraud, Institut des Maladies Neurodégénératives, UMR CNRS 5293, 146, rue Leo Saignat, 33 076 Bordeaux Cedex, France, E-mail: [email protected]Search for more papers by this author
First published: 22 February 2016
Citations: 27

Funding agencies: The project was supported by the Agence Nationale pour la Recherche (ANR-09-SYSC-002-03) and the Centre National pour la Recherche Scientifique (CNRS).

Relevant conflicts of interests/financial disclosures: C.P. was supported by a grant from the Ministry of the Research (14333-2012). D.K. was supported by the Uehara Memorial Foundation and a fellowship from the French government. M.T. was supported by a grant from Inria (14333-2012). T.B., T.N.H., H.O., and M.G. are regular staff members of the CNRS, and N.R. is a regular staff member of INRIA.

ABSTRACT

Background

There is an apparent contradiction between experimental data showing that the basal ganglia are involved in goal-oriented and routine behaviors and clinical observations. Lesion or disruption by deep brain stimulation of the globus pallidus interna has been used for various therapeutic purposes ranging from the improvement of dystonia to the treatment of Tourette's syndrome. None of these approaches has reported any severe impairment in goal-oriented or automatic movement.

Method

To solve this conundrum, we trained 2 monkeys to perform a variant of a 2-armed bandit-task (with different reward contingencies). In the latter we alternated blocks of trials with choices between familiar rewarded targets that elicit routine behavior and blocks with novel pairs of targets that require an intentional learning process.

Results

Bilateral inactivation of the globus pallidus interna, by injection of muscimol, prevents animals from learning new contingencies while performance remains intact, although slower for the familiar stimuli. We replicate in silico these data by adding lateral competition and Hebbian learning in the cortical layer of the theoretical model of the cortex–basal ganglia loop that provided the framework of our experimental approach.

Conclusion

The basal ganglia play a critical role in the deliberative process that underlies learning but are not necessary for the expression of routine movements. Our approach predicts that after pallidotomy or during stimulation, patients should have difficulty with complex decision-making processes or learning new goal-oriented behaviors. © 2016 Movement Disorder Society