Membrane potential oscillations underlying firing patterns in neocortical neurons

Abstract

Membrane potential oscillations were studied in slices of rat somatosensory cortex maintained in vitro, using intracellular recordings from cells in layers case2 3 and 5. The cells were classified according to their firing patterns during long (0.8-1 s) depolarizing current steps. Subthreshold voltage oscillations were revealed by depolarizing the membrane to voltages around threshold for action potentials; however, these were obvious mainly in cells showing marked spike adaptation. When neurons of all firing patterns were stimulated to fire at 40-60 Hz for tens of seconds, spikes abruptly inactivated. Hyperpolarizing the cells by 5-10 mV precipitated pronounced oscillations in 24 out of 35 cells. These oscillations existed in a narrow voltage range, and their frequency varied between 7 and 40 Hz, in a voltage-dependent manner. Spiking frequency was faster than the oscillation frequency for the same membrane potential in a given cell. The Na+ channel blocker tetrodotoxin abolished both the spikes and the oscillations, and blockade of K+ channels by tetraethylammonium converted the oscillations into prolonged and irregular plateaus. Blocking Ca2+ conductance with Co2+ reduced the oscillations amplitude and frequency in two out of three cells. The oscillations that followed spike inactivation varied in amplitude, frequency and persistence among different cells. Layer 5 nonadapting cells possessed the most periodic oscillations, as judged by autocorrelation analysis. Oscillations were also most persistent in this group, maintaining a stable steady-state. In other cell types, the oscillations were less regular and decayed with time. There was no difference among cell groups in the maximal peak to peak amplitude of the oscillations, or their frequency range. It is suggested that the oscillations are generated by ionic conductances that operate within the voltage range just above and below spike threshold, and thus can shape the cells' firing pattern. The prominence of the oscillations in a specific subset of layer 5 cells may indicate the mechanism that underlies the rhythmic firing pattern of those cells. © 1994.