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The Journal of Neuroscience, October 1, 2002, 22(19):8665-8675

The Switch of Subthalamic Neurons From an Irregular to a Bursting Pattern Does Not Solely Depend on Their GABAergic Inputs in the Anesthetic-Free Rat

Nadia Urbain¹, Nicolas Rentéro¹, Damien Gervasoni², Bernard Renaud¹, and Guy Chouvet¹

¹ Laboratoire de Neuropharmacologie et Neurochimie, Institut National de la Santé et de la Recherche Médicale U512, Université Claude-Bernard-Lyon 1, 69373 Lyon, France, and ² Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710

The subthalamic nucleus (STN) powerfully controls basal ganglia outputs and has been implicated in movement disorders observed in Parkinson's disease because of its pathological mixed burst firing mode and hyperactivity. A recent study suggested that reciprocally connected glutamatergic STN and GABAergic globus pallidus (GP) neurons act in vitro as a generator of bursting activity in basal ganglia. In vivo, we reported that GP neurons increased their firing rate in wakefulness (W) compared with slow-wave sleep (SWS) without any change in their random pattern. In contrast, STN neurons exhibited similar firing rates in W and SWS, with an irregular pattern in W and a bursty one in SWS. Thus, the pallidal GABAergic tone might control the STN pattern. This hypothesis was tested by mimicking such variations with microiontophoresis of GABA receptor ligands. GABA agonists specifically decreased the STN firing rate but did not affect its firing pattern. GABA_A (but not GABA_B) antagonists strongly enhanced the STN mean discharge rate during all vigilance states up to three to five times its basal activity. However, such applications did not change the typical W random pattern. When applied during SWS, GABA_A antagonists strongly reinforced the spontaneous bursty pattern into a particularly marked one with instantaneous frequencies reaching 500-600 Hz. SWS-W transitions occurring during ongoing antagonist iontophoresis invariably disrupted the bursty pattern into a random one. Thus GABA_A receptors play a critical, but not exclusive, role in regulating the excitatory STN influence on basal ganglia outputs.

Key words: subthalamic nucleus; GABA; bicuculline; gabazine; extracellular single-unit recordings; firing pattern; bursts of spikes; nonanesthetized animal; sleep-wake cycle; microiontophoresis

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22198665-11$05.00/0

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