Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States

Abstract

Gamma (gamma) oscillation, a hallmark of cortical activity during sensory processing and cognition, occurs during persistent, self-sustained activity or "UP" states, which are thought to be maintained by recurrent synaptic inputs to pyramidal cells. During neocortical "UP" states, excitatory regular spiking (RS) (pyramidal) cells and inhibitory fast spiking (FS) (basket) cells fire with distinct phase distributions relative to the gamma oscillation in the local field potential. Evidence suggests that gamma-modulated RS --> FS input serves to synchronize the interneurons and hence to generate gamma-modulated FS --> RS drive. How RS --> RS recurrent input shapes both self-sustained activity and gamma-modulated phasic firing, although, is unclear. Here, we investigate this by reconstructing gamma-modulated synaptic input to RS cells using the conductance injection (dynamic clamp) technique in cortical slices. We find that, to show lifelike gamma-modulated firing, RS cells require strongly gamma-modulated, low-latency inhibitory inputs from FS cells but little or no gamma-modulation from recurrent RS --> RS connections. We suggest that this demodulation of recurrent excitation, compared with inhibition, reflects several possible effects, including distributed propagation delays and integration of excitation over wider areas of cortex, and maximizes the capacity for representing information by the timing of recurrent excitation.