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J Neurophysiol 86: 2823-2833, 2001;
0022-3077/01 $5.00
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The Journal of Neurophysiology Vol. 86 No. 6 December 2001, pp. 2823-2833
Copyright ©2001 by the American Physiological Society

Disruption of GABAA Receptors on GABAergic Interneurons Leads to Increased Oscillatory Power in the Olfactory Bulb Network

Zoltan Nusser,1,3 Leslie M. Kay,2,5 Gilles Laurent,2 Gregg E. Homanics,4 and Istvan Mody1

 1Department of Neurology, UCLA School of Medicine, Los Angeles 90095-1769;  2Biology Division, California Institute of Technology, Pasadena, California 91125;  3Laboratory of Cellular Neurophysiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083 Budapest, Hungary;  4Departments of Anesthesiology and Pharmacology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15260; and  5Department of Psychology, Institute for Mind and Biology, University of Chicago, Chicago, Illinois 60637

Nusser, Zoltan, Leslie M. Kay, Gilles Laurent, Gregg E. Homanics, and Istvan Mody. Disruption of GABAA Receptors on GABAergic Interneurons Leads to Increased Oscillatory Power in the Olfactory Bulb Network. J. Neurophysiol. 86: 2823-2833, 2001. Synchronized neural activity is believed to be essential for many CNS functions, including neuronal development, sensory perception, and memory formation. In several brain areas GABAA receptor-mediated synaptic inhibition is thought to be important for the generation of synchronous network activity. We have used GABAA receptor beta 3 subunit deficient mice (beta 3-/-) to study the role of GABAergic inhibition in the generation of network oscillations in the olfactory bulb (OB) and to reveal the role of such oscillations in olfaction. The expression of functional GABAA receptors was drastically reduced (>93%) in beta 3-/- granule cells, the local inhibitory interneurons of the OB. This was revealed by a large reduction of muscimol-evoked whole-cell current and the total current mediated by spontaneous, miniature inhibitory postsynaptic currents (mIPSCs). In beta 3-/- mitral/tufted cells (principal cells), there was a two-fold increase in mIPSC amplitudes without any significant change in their kinetics or frequency. In parallel with the altered inhibition, there was a significant increase in the amplitude of theta (80% increase) and gamma (178% increase) frequency oscillations in beta 3-/- OBs recorded in vivo from freely moving mice. In odor discrimination tests, we found beta 3-/- mice to be initially the same as, but better with experience than beta 3+/+ mice in distinguishing closely related monomolecular alcohols. However, beta 3-/- mice were initially better and then worse with practice than control mice in distinguishing closely related mixtures of alcohols. Our results indicate that the disruption of GABAA receptor-mediated synaptic inhibition of GABAergic interneurons and the augmentation of IPSCs in principal cells result in increased network oscillations in the OB with complex effects on olfactory discrimination, which can be explained by an increase in the size or effective power of oscillating neural cell assemblies among the mitral cells of beta 3-/- mice.




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