INTRACELLULAR CORRELATES OF HIPPOCAMPAL THETA-RHYTHM IN IDENTIFIED PYRAMIDAL CELLS, GRANULE CELLS, AND BASKET CELLS

The cellular-synaptic generation of rhythmic slow activity (RSA or the ta) in the hippocampus has been investigated by intracellular recordin g from principal cells and basket cells in anesthetized rats. In addit ion, the voltage-, coherence-, and phase versus depth profiles were ex amined by simultaneously recording field activity at 16 sites in the i ntact rat, during urethane anesthesia, and after bilateral entorhinal cortex lesion. In the extracellular experiments the large peak of thet a at the hippocampal fissure was attenuated by urethane anesthesia and abolished by entorhinal cortex lesion. The phase versus depth profile s were similar during urethane anesthesia and following entorhinal cor tex lesion but distinctly different in the intact, awake rat. These ob servations suggest that dendritic currents underlying theta in the awa ke rat may not be revealed under urethane anesthesia. The frequency of theta-related membrane potential oscillation was voltage-independent in pyramidal neurons, granule cells, and basket cells. On the other ha nd, the phase and amplitude of intracellular theta were voltage-depend ent in all three cell types with an almost complete phase reversal at chloride equilibrium potential in pyramidal cells and basket cells. At strong depolarization levels (less than 30 mV) pyramidal cells emitte d calcium spike oscillations, phase-locked to theta. Basket cells poss essed the most regular membrane oscillations of the three cell types. All neurons of this study were verified by intracellular injection of biocytin. The observations provide direct evidence that theta-related rhythmic hyperpolarization of principal cells is brought about by the rhythmically discharging basket neurons. Furthermore, the finding that basket cells were also paced by rhythmic inhibitory postsynaptic pote ntials during theta suggest that they were periodically hyperpolarized by their GABAergic septal afferents. (C) 1995 Wiley-Liss, Inc.