Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells

Abstract

The cellular‐synaptic generation of rhythmic slow activity (RSA or theta) in the hippocampus has been investigated by intracellular recording from principal cells and basket cells in anesthetized rats. In addition, the voltage‐, coherence‐, and phase versus depth profiles were examined by simultaneously recording field activity at 16 sites in the intact rat, during urethane anesthesia, and after bilateral entorhinal cortex lesion. In the extracellular experiments the large peak of theta at the hippocampal fissure was attenuated by urethane anesthesia and abolished by entorhinal cortex lesion. The phase versus depth profiles were similar during urethane anesthesia and following entorhinal cortex lesion but distinctly different in the intact, awake rat. These observations suggest that dendritic currents underlying theta in the awake 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 hand, the phase and amplitude of intracellular theta were voltage‐dependent 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 emitted calcium spike oscillations, phase‐locked to theta. Basket cells possessed 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 potentials during theta suggest that they were periodically hyperpolarized by their GABAergic septal afferents. & 1995 Wiley‐Liss, Inc.