THETA-OSCILLATION IN SOMATA AND DENDRITES OF HIPPOCAMPAL PYRAMIDAL CELLS IN-VIVO - ACTIVITY-DEPENDENT PHASE-PRECESSION OF ACTION-POTENTIALS

Theta frequency field oscillation reflects synchronized synaptic poten tials that entrain the discharge of neuronal populations within the si milar to 100-200 ms range. The cellular-synaptic generation of theta a ctivity in the hippocampus was investigated by intracellular recording s from the somata and dendrites of CA1 pyramidal cells in urethane-ane sthetized rats. The recorded neurons were verified by intracellular in jection of biocytin. Transition from non-theta to theta state was char acterized by a large decrease in the input resistance of the neuron (3 9% in the soma), tonic somatic hyperpolarization and dendritic depolar ization. The probability of pyramidal cell discharge, as measured in s ingle cells and from a population of extracellularly recorded units, w as highest at or slightly after the negative peak of the field theta r ecorded from the pyramidal layer. In contrast, cyclic depolarizations in dendrites corresponded to the positive phase of the pyramidal layer field theta (i.e. the hyperpolarizing phase of somatic theta). Curren t-induced depolarization of the dendrite triggered large amplitude slo w spikes (putative Ca2+ spikes) which were phase-locked to the positiv e phase of field theta. In the absence of background theta, strong den dritic depolarization by current injection led to large amplitude, sel f-sustained oscillation in the theta frequency range. Depolarization o f the neuron resulted in a voltage-dependent phase precession of the a ction potentials. The voltage-dependent phase-precession was replicate d by a two-compartment conductance model. Using an active (bursting) d endritic compartment spike phase advancement of action potentials, rel ative to the somatic theta rhythm, occurred up to 360 degrees. These d ata indicate that distal dendritic depolarization of the pyramidal cel l by the entorhinal input during theta overlaps in time with somatic h yperpolarization. As a result, most pyramidal cells are either silent or discharge with single spikes on the negative portion of local field theta (i.e., when the somatic region is least polarized). However, st rong dendritic excitation may overcome perisomatic inhibition and the large depolarizing theta rhythm in the dendrites may induce spike burs ts at an earlier phase of the extracellular theta cycle. The magnitude of dendritic depolarization is reflected by the timing of action pote ntials within the theta cycle. We hypothesize that the competition bet ween the out-of-phase theta oscillation ion in the soma and dendrite i s responsible for the advancement of spike discharges observed in the behaving animal. Hippocampus 1998;8:244-261. (C) 1998 Wiley-Liss, Inc.