Disinhibition of hippocampal pyramidal cells during the transition into theta rhythm

The activity of hippocampal complex-spike cells (presumed pyramidal cells) and theta cells (presumed interneurons) was examined during transitions from non-theta electroencephalogram (EEG) states to theta EEG states in freely moving and sleeping rats. Theta cell firing rates were significantly depressed in a 1-s period centered on the EEG transition relative to the surrounding 1-s periods (normalized rates +/- SEM): 1.05 +/- 0.02 for the "non-theta" period, 0.59 +/- 0.03 for the "transition" period, and 1.36 +/- 0.04 for the "theta" period (n = 26 cells). Conversely, complex-spike cell firing was significantly increased during the transition period: 0.51 +/- 0.11 for the "non-theta" period, 2.24 +/- 0.19 for the "transition" period, and 0.24 +/- 0.04 for the "theta" period (n = 27 cells). This diametrically altered activity indicates that theta cells must be actively inhibited during the transition. The increased activity in complex-spike cells during the transition may be simply a release from inhibitory control by interneurons. The pattern of theta cell inhibition together with increased complex-spike cell activity appears to be a general property of transitions into the theta EEG state, irrespective of behavior. It is suggested that increased activity in septal afferents (GA-BAergic cell activity greater than cholinergic cell activity) initially inhibits hippocampal interneurons. The inhibition is not sustained because of an activity-dependent decrease in the potency of the septointerneuronal inhibition, leaving the rhythmic excitatory (cholinergic) septointerneuronal inputs, together with principal cell inputs, to increase interneuron firing rates.