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The Journal of Neuroscience, March 29, 2006, 26(13):3567-3583; doi:10.1523/JNEUROSCI.5050-05.2006

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Behavioral/Systems/Cognitive
Competition between Feedback Loops Underlies Normal and Pathological Dynamics in the Basal Ganglia

Arthur Leblois,^1,2,4 Thomas Boraud,^2,4 Wassilios Meissner,² Hagai Bergman,^3,4 and David Hansel^1,4

¹Laboratoire de Neurophysique et Physiologie du Système Moteur, Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 8119, Université René Descartes, 75270 Paris, France, ²Basal Gang, Laboratoire de Neurophysiologie, CNRS UMR 5543, Université Victor Segalen, 33076 Bordeaux, France, ³Interdisciplinary Center for Neural Computation, The Hebrew University, Jerusalem 91904, Israel, and ⁴Laboratoire Franco-Israelien de Neurophysiologie et Neurophysique des Systèmes, Université René Descartes, 75270 Paris, France

Correspondence should be addressed to David Hansel, Laboratoire de Neurophysique et Physiologie du Système Moteur, 45 rue des Saints-Pères, 75270 Paris, France. Email: David.Hansel{at}biomedicale.univ-Paris5.fr

Experiments performed in normal animals suggest that the basal ganglia (BG) are crucial in motor program selection. BG are also involved in movement disorders. In particular, BG neuronal activity in parkinsonian animals and patients is more oscillatory and more synchronous than in normal individuals.

We propose a new model for the function and dysfunction of the motor part of BG. We hypothesize that the striatum, the subthalamic nucleus, the internal pallidum (GPi), the thalamus, and the cortex are involved in closed feedback loops. The direct (cortex–striatum–GPi–thalamus–cortex) and the hyperdirect loops (cortex–subthalamic nucleus–GPi–thalamus–cortex), which have different polarities, play a key role in the model. We show that the competition between these two loops provides the BG–cortex system with the ability to perform motor program selection. Under the assumption that dopamine potentiates corticostriatal synaptic transmission, we demonstrate that, in our model, moderate dopamine depletion leads to a complete loss of action selection ability. High depletion can lead to synchronous oscillations. These modifications of the network dynamical state stem from an imbalance between the feedback in the direct and hyperdirect loops when dopamine is depleted.

Our model predicts that the loss of selection ability occurs before the appearance of oscillations, suggesting that Parkinson's disease motor impairments are not directly related to abnormal oscillatory activity. Another major prediction of our model is that synchronous oscillations driven by the hyperdirect loop appear in BG after inactivation of the striatum.

Key words: neural network; models; action selection; oscillations; synchrony; Parkinson's disease

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Received Oct. 7, 2005; revised Feb. 9, 2006; accepted Feb. 9, 2006.

Correspondence should be addressed to David Hansel, Laboratoire de Neurophysique et Physiologie du Système Moteur, 45 rue des Saints-Pères, 75270 Paris, France. Email: David.Hansel{at}biomedicale.univ-Paris5.fr

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J. Neurosci. 2006 26: 7317-7318. [Full Text]  

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