Differential expression of synaptic and nonsynaptic mechanisms underlying stimulus-induced gamma oscillations in vitro

Gamma frequency oscillations occur in hippocampus in vitro after brief teta ni delivered to afferent pathways. Previous reports have characterized thes e oscillations as either (1) trains of GABA(A) inhibitory synaptic events m ediated 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 inhib itory synaptic oscillation when cells are driven by depolarizing GABA respo nses and local synchrony is produced by field effects. The aim of this stud y was to investigate factors involved in the differential expression of the se 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 synapti c events associated with an oscillation and enhanced the depolarizing GABA component underlying the post-tetanic depolarization. The resulting field o scillation was still dependent, at least in part, on inhibitory synaptic tr ansmission, but spatiotemporal aspects of the oscillation were severely dis rupted. 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 lat ter remain a viable model for in vivo oscillations of cognitive relevance.