Relationship Between Membrane Potential Oscillations and Rhythmic Discharges in Identified Hippocampal Theta-Related Cells

Abstract

Intracellular recordings of cells, classified according to the criteria of Colom and Bland as phasic theta-on or phasic theta-off cells, were carried out in the dorsal region of the hippocampal formation in urethan-anesthetized rats. Cells were studied during two spontaneously occurring hippocampal field conditions, asynchrony, termed large-amplitude irregular activity, and synchrony, termed theta. During the spontaneous cycling between these two field states, the effect of four levels of intracellular depolarizing and hyperpolarizing constant current injections on the amplitude and phase of membrane potential oscillations (MPOs) and the rate and pattern of cell discharges was assessed. Labeled CA1 pyramidal cells and bistratified cells met the criteria for classification as phasic theta-on cells and labeled CA1 pyramidal layer basket cells, mossy hilar cells, and granule cells met the criteria for classification as phasic theta-off cells. MPOs were recorded in CA1 pyramidal cells, CA1 layer basket cells, mossy interneurons, and granule cells only during theta field activity, their onset in theta-on cells signaled by a depolarizing shift of 5–10 mV and in theta-off cells by a hyperpolarizing shift of 5–10 mV, in membrane potential. The effect of current injections in phasic theta-on and theta-off cells during the theta field condition revealed that MPO amplitude was voltage dependent and frequency was voltage independent. There were no phase changes observed in phasic theta-on cells during current injections; however, amplitude analysis revealed an inverted U-shaped curve asymmetrically distributed around the average value of the membrane potential occurring during the spontaneous theta (no current) control condition. The occurrence and rate of rhythmical cell discharges in CA1 pyramidal phasic theta-on cells during the theta condition was precisely controlled within a critical range of membrane potential values from approximately −57 to −68 mV, corresponding to a range of MPO amplitudes of ∼4–7 mV. Outside the critical range, rhythmic cell discharges were abolished. Membrane potential oscillations in CA1 pyramidal layer basket cells underwent an approximate 180° phase reversal when the membrane potential was depolarized above −65 mV. The occurrence and rate of rhythmic cell discharges in CA1 pyramidal layer basket cell phasic theta-off cells during the theta condition was precisely controlled within a critical range of membrane potential values from approximately −62 to −60 mV, corresponding to a range of MPO amplitudes of ∼7–7.5 mV. Outside the critical range, cell discharges were absent or occurred singly.