Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity-dependent phase-precession of action potentials

Abstract

Theta frequency field oscillation reflects synchronized synaptic potentials that entrain the discharge of neuronal populations within the D100-200 ms range. The cellular-synaptic generation of theta activity in the hippocampus was investigated by intracellular recordings from the somata and dendrites of CA1 pyramidal cells in urethaneanesthetized rats. The recorded neurons were verified by intracellular injection of biocytin. Transition from non-theta to theta state was characterized by a large decrease in the input resistance of the neuron (39% in the soma), tonic somatic hyperpolarization and dendritic depolarization. The probability of pyramidal cell discharge, as measured in single cells and from a population of extracellularly recorded units, was highest at or slightly after the negative peak of the field theta recorded 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). Current-induced depolarization of the dendrite triggered large amplitude slow spikes (putative Ca 2؉ spikes) which were phase-locked to the positive phase of field theta. In the absence of background theta, strong dendritic depolarization by current injection led to large amplitude, self-sustained oscillation in the theta frequency range. Depolarization of the neuron resulted in a voltagedependent phase precession of the action potentials. The voltagedependent phase-precession was replicated by a two-compartment conductance model. Using an active (bursting) dendritic compartment spike phase advancement of action potentials, relative to the somatic theta rhythm, occurred up to 360 degrees. These data indicate that distal dendritic depolarization of the pyramidal cell by the entorhinal input during theta overlaps in time with somatic hyperpolarization. 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, strong dendritic excitation may overcome perisomatic inhibition and the large depolarizing theta rhythm in the dendrites may induce spike bursts at an earlier phase of the extracellular theta cycle. The magnitude of dendritic depolarization is reflected by the timing of action potentials within the theta cycle. We hypothesize that the competition between the out-of-phase theta oscillation in the soma and dendrite is responsible for the advancement of spike discharges observed in the behaving animal.

Phase Precession Through Synaptic Facilitation

“…Some of the single cell models assume that precession arises in CA1 (Kamondi et al, 1998;Magee, 2001;Harris et al, 2002;Mehta et al, 2002). Another class of phase precession models explicitly requires a network of neurons.…”

“…To be more specific, hippocampal pyramidal cells exhibit membrane potential oscillations in the theta range, which reflect the electroencephalogram (EEG) theta oscillations of the field potential. Intracellular theta oscillations have amplitudes of up to 10 mV in anesthetized animals (Kamondi, Acsady, Wang, & Buzsáki, 1998;Bland, Konopacki, & Dyck, 2005), and were also observed in behaving animals (Lee, Manns, Sakmann, & Brecht, 2006). The maximum of the somatic membrane potential oscillation corresponds to the minimum of the EEG in the stratum pyramidale (Kamondi et al, 1998), which is defined as 0 degree in accordance with Csicsvari, Hirase, Czurkó, Mamiya, and Buzsáki (1999) and Buzsáki (2002).…”

“…In this letter we explain how phase precession can be generated in single cells, which is similar to the approaches of O'Keefe and Recce (1993), Kamondi et al (1998), Magee (2001), Harris et al (2002), Mehta et al (2002), Lengyel et al (2003), and Huhn et al (2005). Some of the single cell models assume that precession arises in CA1 (Kamondi et al, 1998;Magee, 2001;Harris et al, 2002;Mehta et al, 2002).…”

Interaction between neocortical and hippocampal networks via slow oscillations

“…Perforant path input to distal dendrites of the CA1 and CA3 pyramidal cells and dentate granule cells is believed to produce current dipoles that are responsible for the large amplitude of theta at around the hippocampal fissure (Buzsáki et al, 1983). This latter oscillator is atropine-resistant, but is abolished by urethane anesthesia and lesions of the entorhinal cortex and originates mainly in layers 2/3 of the entorhinal cortex Ylinen et al, 1995b;Kamondi et al, 1998). In support of this hypothesis, many layer 2/3 cells of the entorhinal cortex are phase-locked to the hippocampal theta (Alonso and Garcia-Austt, 1987b;Chrobak and Buzsáki, 1998b;Alonso and Llinás, 1989), and the theta waveshape reverses around layer 2 of the entorhinal cortex (Alonso and Garcia-Austt, 1987a;Mitchell and Ranck, 1980).…”

The role of ongoing dendritic oscillations in single-neuron dynamics

“…In entorhinal cortex stellate cells, experiments have shown that the oscillations result from an interaction of the persistent sodium current I NaP and the hyperpolarization activated inward current I h [6,13,14]. Recordings from hippocampal CA1 pyramidal neurons have also demonstrated ongoing oscillations in the dendrites that include repetitive dendritic spikes, presumably involving Ca 2+ currents [15].…”