Layer‐specific pyramidal cell oscillations evoked by tetanic stimulation in the rat hippocampal area CA1 in vitro and in vivo

Abstract

Tetanic stimulation of axons terminating in the CA1 region of the hippocampus induces oscillations in the gamma-to-beta frequency band (13-100 Hz) and can induce long-term potentiation (LTP). The rapid pyramidal cell discharge is driven by a mainly GABA(A)-receptor-mediated slow depolarization and entrained mainly through ephaptic interactions. This study tests whether cellular compartmentalization can explain how cells, despite severely reduced input resistance, can still fire briskly and have IPSPs superimposed on the slow GABAergic depolarization, and whether this behaviour occurs in vivo. Oscillations induced in CA1 in vitro by tetanic stimulation of the stratum radiatum or oriens were analysed using intracellular and multichannel field potentials along the cell axis. Layer-specific effects of focal application of bicuculline indicate that the GABAergic depolarization is concentrated on tetanized dendrites. Current-source density analysis and characteristics of partial spikes indicate that early action potentials are initiated in the proximal nontetanized dendrite but cannot invade the tetanized dendrite, where recurrent EPSPs and evoked IPSPs were largely suppressed. As the oscillation progresses, IPSPs recover and slow the neuronal firing to beta frequencies, with a small subpopulation of neurons continuing to fire at gamma frequency. Carbonic anhydrase dependence, threshold intensity, frequency, field strength and spike initiation/propagation of tetanus-evoked oscillations in urethane-anaesthetized rats, validate our observations in vitro, and show that these mechanisms operate in healthy tissue. However, the disrupted electrophysiology of the tetanized dendrites will disable normal information processing, has implications for LTP induction and is likely to play a role in pathological synchronization as found during epileptic discharges.