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The Journal of Neuroscience, March 7, 2007, 27(10):2525-2538; doi:10.1523/JNEUROSCI.4156-06.2007

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Behavioral/Systems/Cognitive
Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Shlomo Elias,¹ Mati Joshua,^1,2 Joshua A. Goldberg,^1,2 Gali Heimer,¹ David Arkadir,¹ Genela Morris,^1,2 and Hagai Bergman^1,2,3

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

Correspondence should be addressed to Shlomo Elias, Department of Physiology, The Hebrew University–Hadassah Medical School, P.O. Box 12272, 91120 Jerusalem, Israel. Email: shlomoe{at}md.huji.ac.il

The neurons of many basal ganglia nuclei, including the external and internal globus pallidus (GPe and GPi, respectively) and the substantia nigra pars reticulata (SNr) are characterized by their high-frequency (50–100 spikes/s) tonic discharge (HFD). However, the high firing rate of GPe neurons is interrupted by long pauses. We studied the extracellularly recorded spiking activity of 212 well-isolated HFD GPe and 52 GPi/SNr neurons from five monkeys during different states of behavioral activity. An algorithm that maximizes the surprise function was used to detect pauses and pauser cells ("pausers"). Only 6% of the GPi/SNr neurons versus as many as 56% of the GPe neurons were classified as pausers. The GPe average pause duration equals 0.62 s. The interpause intervals follow a Poissonian distribution with a frequency of 13 pauses/minute. No linear relationship was found between pause parameters (duration or frequency) and the firing rate of the cell. Pauses were preceded by various changes in firing rate but not dominantly by a decrease. The average amplitude and duration of the spike waveform was modulated only after the pause but not before it. Pauses of pairs of cells that were recorded simultaneously were not correlated. The probability of GPe cells to pause spontaneously was extremely variable among monkeys (30–90%) and inversely related to the degree of the monkey's motor activity. These findings suggest that spontaneous GPe pauses are related to low-arousal periods and are generated by a process that is independent of the discharge properties of the cells.

Key words: primate; basal ganglia; firing pattern; correlation; spikes; arousal

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Received June 23, 2006; revised Jan. 25, 2006; accepted Jan. 26, 2007.

Correspondence should be addressed to Shlomo Elias, Department of Physiology, The Hebrew University–Hadassah Medical School, P.O. Box 12272, 91120 Jerusalem, Israel. Email: shlomoe{at}md.huji.ac.il

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