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The Journal of Neuroscience, March 1, 2001, 21(5):1727-1738

Differential Expression of Synaptic and Nonsynaptic Mechanisms Underlying Stimulus-Induced Gamma Oscillations In Vitro

M. A. Whittington¹, H. C. Doheny^{1, 2}, R. D. Traub³, F. E. N. LeBeau¹, and E. H. Buhl¹

¹ School of Biomedical Sciences, University of Leeds, Leeds LS2 9NL, United Kingdom, ² Division of Neuroscience and Psychological Medicine, Imperial College, London W6 8RP, United Kingdom, and ³ Division of Neuroscience, University of Birmingham Medical School, Birmingham B15 2TT, United Kingdom

Gamma frequency oscillations occur in hippocampus in vitro after brief tetani delivered to afferent pathways. Previous reports have characterized these oscillations as either (1) trains of GABA_A inhibitory synaptic events mediated by depolarization of both pyramidal cells and interneurons at least in part mediated by metabotropic glutamate and acetylcholine receptors, or (2) field potential oscillations occurring in the near absence of an inhibitory synaptic oscillation when cells are driven by depolarizing GABA responses and local synchrony is produced by field effects. The aim of this study was to investigate factors involved in the differential expression of these synaptically and nonsynaptically gated oscillations. Field effects were undetectable in control recordings but manifested when slices were perfused with hypo-osmotic solutions or a reduced level of normal perfusate. These manipulations also reduced the amplitude of the train of inhibitory synaptic events associated with an oscillation and enhanced the depolarizing GABA component underlying the post-tetanic depolarization. The resulting field oscillation was still dependent, at least in part, on inhibitory synaptic transmission, but spatiotemporal aspects of the oscillation were severely disrupted. These changes were also accompanied by an increase in estimated [K⁺]_o compared with control. We suggest that nonsynaptic oscillations occur under conditions also associated with epileptiform activity and constitute a phenomenon that is distinct from synaptically gated oscillations. The latter remain a viable model for in vivo oscillations of cognitive relevance.

Key words: gamma oscillation; tetanic stimulation; synaptic potentials; ephaptic effects; osmotic changes; potassium ion concentrations

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Copyright © 2001 Society for Neuroscience  0270-6474/01/2151727-12$05.00/0

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