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The Journal of Neuroscience, August 17, 2005, 25(33):7687-7696; doi:10.1523/JNEUROSCI.1056-05.2005

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Neurobiology of Disease
Neuroleptic-Induced Catalepsy: Electrophysiological Mechanisms of Functional Recovery Induced by High-Frequency Stimulation of the Subthalamic Nucleus

Bertrand Degos,¹ Jean-Michel Deniau,¹ Anne-Marie Thierry,² Jacques Glowinski,² Laurent Pezard,³ and Nicolas Maurice¹

¹Institut National de la Santé et de la Recherche Médicale Unité 667 and ²Unité 114/Chaire de Neuropharmacologie, Collège de France, 75231 Paris Cedex 05, France, and ³Centre National de la Recherche Scientifique Unité Propre de Recherche 640-Laboratoire de Neurosciences Cognitives et Imagerie Cérébrale, Hôpital de la Salpêtrière, 75651 Paris Cedex 13, France

High-frequency stimulation (HFS) of the subthalamic nucleus (STN) remarkably alleviates motor disorders in parkinsonian patients. The mechanisms by which STN HFS exerts its beneficial effects were investigated in anesthetized rats, using a model of acute interruption of dopaminergic transmission. Combined systemic injections of SCH-23390 [R(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5,-tetrahydro-1H-3-benzazepine] and raclopride, antagonists of the D₁ and D₂ classes of dopaminergic receptors, respectively, were performed, and the parameters of STN HFS that reversed the neuroleptic-induced catalepsy were determined in freely moving animals. The effects of neuroleptics and the impact of STN HFS applied at parameters alleviating neuroleptic-induced catalepsy were analyzed in the substantia nigra pars reticulata (SNR), a major basal ganglia output structure, by recording the neuronal firing pattern and the responses evoked by cortical stimulation. Neuroleptic injection altered the tonic and regular mode of discharge of SNR neurons, most of them becoming irregular with bursts of spikes and pauses. The inhibitory component of the cortically evoked response, which is attributable to the activation of the direct striatonigral circuit, was decreased, whereas the late excitatory response resulting from the indirect striato-pallido-subthalamo-nigral circuit was reinforced. During STN HFS, the spontaneous firing of SNR cells was either increased or decreased with a global enhancement of the firing rate in the overall population of SNR cells recorded. However, in all of the cases, SNR firing pattern was regularized, and the bias between the trans-striatal and trans-subthalamic circuits was reversed. By these effects, STN HFS restores the functional properties of the circuits by which basal ganglia contribute to motor activity.

Key words: substantia nigra pars reticulata; basal ganglia; deep brain stimulation; Parkinson's disease; neuronal activity; dopaminergic transmission

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Received March 18, 2005; revised July 5, 2005; accepted July 11, 2005.

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