Self-organized synaptic plasticity contributes to the shaping of γ and β oscillations in vitro

Abstract

γ(30-70 Hz) followed by β (10-30 Hz) oscillations are evoked in humans by sensory stimuli and may be involved in working memory. Phenomenologically similar γ→β oscillations can be evoked in hippocampal slices by strong two-site tetanic stimulation. Weaker stimulation leads only to two-site synchronized γ. In vitro oscillations have memory-like features: (1) EPSPs increase during γ→β; (2) after a strong one-site stimulus, two-site stimulation produces desynchronized γ; and (3) a single synchronized γ→β epoch allows a subsequent weak stimulus to induce synchronized γ→β. Features 2 and 3 last > 50 min and so are unlikely to be caused by presynaptic effects. A previous model replicated the γ→β 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 pyramidal→pyramidal and pyramidal→interneuron synapses are modifiable. This model, in a self-organized way, replicates the γ→β 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 γ oscillations is to permit synaptic plasticity, which is then expressed in the form of β oscillations. We propose that the period of γ oscillations, ∼25 msec, is "designed" to match the time course of [Ca2+]i fluctuations in dendrites, thus facilitating learning.