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The Journal of Neuroscience, November 15, 2001, 21(22):9053-9067

Self-Organized Synaptic Plasticity Contributes to the Shaping of gamma  and beta  Oscillations In Vitro

Andrea Bibbig1, 4, Howard J. Faulkner2, Miles A. Whittington3, and Roger D. Traub1, 4

1 Department of Pharmacology, University of Birmingham School of Medicine, Edgbaston, Birmingham B15 2TT, United Kingdom, 2 Imperial College School of Medicine, London SW7 2AZ, United Kingdom, 3 School of Biomedical Sciences, University of Leeds, Leeds LS2 9NQ, United Kingdom, and 4 Department of Physiology and Pharmacology, State University of New York Health Science Center, Brooklyn, New York 11203

gamma (30-70 Hz) followed by beta  (10-30 Hz) oscillations are evoked in humans by sensory stimuli and may be involved in working memory. Phenomenologically similar gamma right-arrowbeta oscillations can be evoked in hippocampal slices by strong two-site tetanic stimulation. Weaker stimulation leads only to two-site synchronized gamma . In vitro oscillations have memory-like features: (1) EPSPs increase during gamma right-arrowbeta ; (2) after a strong one-site stimulus, two-site stimulation produces desynchronized gamma ; and (3) a single synchronized gamma right-arrowbeta epoch allows a subsequent weak stimulus to induce synchronized gamma right-arrowbeta . Features 2 and 3 last >50 min and so are unlikely to be caused by presynaptic effects. A previous model replicated the gamma right-arrowbeta transition when it was assumed that K+ conductance(s) increases and there is an ad hoc increase in pyramidal EPSCs. Here, we have refined the model, so that both pyramidalright-arrowpyramidal and pyramidalright-arrowinterneuron synapses are modifiable. This model, in a self-organized way, replicates the gamma right-arrowbeta transition, along with features 1 and 2 above. Feature 3 is replicated if learning rates, or the time course of K+ current block, are graded with stimulus intensity. Synaptic plasticity allows simulated oscillations to synchronize between sites separated by axon conduction delays over 10 msec. Our data suggest that one function of gamma  oscillations is to permit synaptic plasticity, which is then expressed in the form of beta  oscillations. We propose that the period of gamma  oscillations, ~25 msec, is "designed" to match the time course of [Ca2+]i fluctuations in dendrites, thus facilitating learning.

Key words: Hebbian synapses; 40 Hz; synchronization; EEG; learning; memory


Copyright © 2001 Society for Neuroscience  0270-6474/01/21229053-15$05.00/0


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