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Science 3 October 1997:
Vol. 278. no. 5335, pp. 130 - 134
DOI: 10.1126/science.278.5335.130
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Reports

Functional Dynamics of GABAergic Inhibition in the Thalamus

Uhnoh Kim, Maria V. Sanchez-Vives, David A. McCormick *

The inhibitory gamma -aminobutyric acid-containing (GABAergic) neurons of the thalamic reticular and perigeniculate nuclei are involved in the generation of normal and abnormal synchronized activity in thalamocortical networks. An important factor controlling the generation of activity in this system is the amplitude and duration of inhibitory postsynaptic potentials (IPSPs) in thalamocortical cells, which depend on the pattern of activity generated in thalamic reticular and perigeniculate cells. Activation of single ferret perigeniculate neurons generated three distinct patterns of GABAergic IPSPs in thalamocortical neurons of the dorsal lateral geniculate nucleus: Low-frequency tonic discharge resulted in small-amplitude IPSPs mediated by GABAA receptors, burst firing resulted in large-amplitude GABAA IPSPs, and prolonged burst firing activated IPSPs mediated by GABAA and GABAB receptors. These functional properties of GABAergic inhibition can reconfigure the operations of thalamocortical networks into patterns of activity associated with waking, slow-wave sleep, and generalized seizures.

Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510, USA.
*   To whom correspondence should be addressed. E-mail: david.mccormick{at}yale.edu

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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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