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The Journal of Neuroscience, July 6, 2005, 25(27):6304-6315; doi:10.1523/JNEUROSCI.0450-05.2005

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Behavioral/Systems/Cognitive
Globus Pallidus Neurons Dynamically Regulate the Activity Pattern of Subthalamic Nucleus Neurons through the Frequency-Dependent Activation of Postsynaptic GABA_A and GABA_B Receptors

Nicholas E. Hallworth and Mark D. Bevan

Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois 60611-3008

Reciprocally connected GABAergic neurons of the globus pallidus (GP) and glutamatergic neurons of the subthalamic nucleus (STN) are a putative generator of pathological rhythmic burst firing in Parkinson's disease (PD). Burst firing of STN neurons may be driven by rebound depolarization after barrages of GABA_A receptor (GABA_AR)-mediated IPSPs arising from pallidal fibers. To determine the conditions under which pallidosubthalamic transmission activates these and other postsynaptic GABARs, a parasagittal mouse brain slice preparation was developed in which pallidosubthalamic connections were preserved. Intact connectivity was first confirmed through the injection of a neuronal tracer into the GP. Voltage-clamp and gramicidin-based perforated-patch current-clamp recordings were then used to study the relative influences of GABA_AR- and GABA_BR-mediated pallidosubthalamic transmission on STN neurons. Spontaneous phasic, but not tonic, activation of postsynaptic GABA_ARs reduced the frequency and disrupted the rhythmicity of autonomous firing in STN neurons. However, postsynaptic GABA_BRs were only sufficiently activated to impact STN firing when pallidosubthalamic transmission was elevated or pallidal fibers were synchronously activated by electrical stimulation. In a subset of neurons, rebound burst depolarizations followed high-frequency, synchronous stimulation of pallidosubthalamic fibers. Although GABA_BR-mediated hyperpolarization was itself sufficient to generate rebound bursts, coincident activation of postsynaptic GABA_ARs produced longer and more intense burst firing. These findings elucidate a novel route through which burst activity can be generated in the STN, and suggest that GABARs on STN neurons could act in a synergistic manner to generate abnormal burst activity in PD.

Key words: basal ganglia; network; synchrony; burst; synaptic transmission; Parkinson's disease

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Received Feb 2, 2005; revised April 12, 2005; accepted May 19, 2005.

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