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Science 299 (5614): 1902-1905

Copyright © 2003 by the American Association for the Advancement of Science

Identified Sources and Targets of Slow Inhibition in the Neocortex

Gábor Tamás,* Andrea Lőrincz, Anna Simon, János Szabadics

There are two types of inhibitory postsynaptic potentials in the cerebral cortex. Fast inhibition is mediated by ionotropic gamma -aminobutyric acid type A (GABAA) receptors, and slow inhibition is due to metabotropic GABAB receptors. Several neuron classes elicit inhibitory postsynaptic potentials through GABAA receptors, but possible distinct sources of slow inhibition remain unknown. We identified a class of GABAergic interneurons, the neurogliaform cells, that, in contrast to other GABA-releasing cells, elicited combined GABAA and GABAB receptor-mediated responses with single action potentials and that predominantly targeted the dendritic spines of pyramidal neurons. Slow inhibition evoked by a distinct interneuron in spatially restricted postsynaptic compartments could locally and selectively modulate cortical excitability.

Department of Comparative Physiology, University of Szeged, Közép fasor 52, Szeged H-6726, Hungary.
*   To whom correspondence should be addressed. E-mail: gtamas{at}bio.u-szeged.hu

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