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The Journal of Neuroscience, September 21, 2005, 25(38):8611-8619; doi:10.1523/JNEUROSCI.1719-05.2005

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Behavioral/Systems/Cognitive
Balance of Monosynaptic Excitatory and Disynaptic Inhibitory Responses of the Globus Pallidus Induced after Stimulation of the Subthalamic Nucleus in the Monkey

Hitoshi Kita,¹ Yoshihisa Tachibana,² Atsushi Nambu,² and Satomi Chiken¹

¹Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, Memphis, Tennessee 38163, and ²Division of System Neurophysiology, National Institute for Physiological Sciences, and School of Life Science, The Graduate University for Advanced Studies, Myodaiji, Okazaki 444-8585, Japan

The subthalamic nucleus (STN) plays a pivotal role in controlling the activity of both the external and internal segments of the globus pallidus (GPe and GPi, respectively). Both nuclei receive monosynaptic excitatory and disynaptic GPe-mediated inhibitory inputs from the STN. Thus, we investigated the balance of these antagonistic inputs that may determine the overall response of pallidum to STN activation in monkeys. Single stimulation of the STN evoked a short-latency excitation followed by a weak inhibition in GPe neurons and a short-latency, very short-duration excitation followed by a strong inhibition in GPi neurons. Burst high-frequency stimulation (BHFS) (10 stimuli with 100 Hz) of the STN (STN-BHFS) evoked powerful excitatory responses in GPe neurons. Local injection of a mixture of 1, 2, 3, 4-tetrahydro-6-nitro-2, 3-dioxobenzo[f]quinoxaline-7-sulfonamide (NBQX; AMPA/kainate receptor blocker) and 3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP; NMDA receptor blocker) greatly diminished or abolished excitatory responses to the STN stimulation. In contrast to the GPe, STN-BHFS evoked a predominantly inhibitory response in GPi neurons. The inhibition could be blocked either by a local application of the GABA_A receptor antagonist gabazine or by an injection of an NBQX/CPP/gabazine mixture into the GPe. STN-BHFS induced weak excitatory or inhibitory responses in a small number of phasically active putamen neurons. These data suggest that with single stimulation and during STN-BHFS, the STN-GPe excitatory response dominates over the STN-GPe-GPe recurrent inhibition in the GPe, whereas the STN-GPe-GPi inhibitory response dominates over the STN-GPi excitatory response in the GPi.

Key words: globus pallidus; subthalamic nucleus; unit recording; glutamatergic responses; GABAergic responses; awake monkey

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Received April 29, 2005; revised July 2, 2005; accepted August 9, 2005.

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