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The Journal of Neuroscience, August 18, 2004, 24(33):7410-7419; doi:10.1523/JNEUROSCI.1691-04.2004

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Neurobiology of Disease
Complex Locking Rather Than Complete Cessation of Neuronal Activity in the Globus Pallidus of a 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine-Treated Primate in Response to Pallidal Microstimulation

Izhar Bar-Gad,^1,2 Shlomo Elias,² Eilon Vaadia,^1,2 and Hagai Bergman^1,2,3

¹Center for Neural Computation, The Hebrew University, Jerusalem 91904, Israel, ²Department of Physiology, Hadassah Medical School, The Hebrew University, Jerusalem 91120, Israel, and ³Eric Roland Center for Neurodegenerative Diseases, The Hebrew University, Jerusalem 91904, Israel

High-frequency stimulation of the globus pallidus (GP) has emerged as a successful tool for treating Parkinson's disease and other motor disorders. However, the mechanism governing its therapeutic effect is still under debate. To shed light on the basic mechanism of deep brain stimulation (DBS), we performed microstimulation in the GP of a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated monkey while recording with other microelectrodes in the same nucleus. We used robust methods to reduce the stimulus artifact, and 600-3000 repetitions of a single stimulus and of high-frequency short trains (10-40 stimuli), enabling high temporal resolution analysis of neural responses. Low-frequency stimulation yielded a typical three-stage response: short-term (2-3 msec duration) activity, followed by mid-term (15-25 msec) inhibition, and occasionally longer-term (30-40 msec) excitation. Trains of high-frequency stimuli elicited complex locking of the response to the stimuli in most neurons. The locking displayed a stereotypic temporal structure consisting of three short-duration (1-2 msec) phases: an initial (mean latency = 2.9 msec) excitation followed by an inhibition (4.6 msec) and a second excitation (6.3 msec). The change in the mean firing rate was mixed; the majority of the neurons displayed partial inhibition during the stimulus train. Slow inhibitory and excitatory multiphase changes in the firing rate were observed after the stimulus trains. The activity of neurons recorded simultaneously displayed rate correlations but no spike-to-spike correlations. Our results suggest that the effect of DBS on the GP is not complete inhibition but rather a complex reshaping of the temporal structure of the neuronal activity within that nucleus.

Key words: basal ganglia; high-frequency stimulation; Parkinson's disease; deep brain stimulation; stimulus artifact; extracellular recording; MPTP

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Received May 4, 2004; revised July 13, 2004; accepted July 13, 2004.

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