Synchronization of Firing in Cortical Fast-Spiking Interneurons at Gamma Frequencies: A Phase-Resetting Analysis

Nathan W Gouwens,Kazuyuki Aihara,Hugh P C Robinson,Hugo Zeberg,Takashi Tateno,Kunichika Tsumoto,Lyle J Graham

doi:10.1371/journal.pcbi.1000951

Abstract

Fast-spiking (FS) cells in the neocortex are interconnected both by inhibitory chemical synapses and by electrical synapses, or gap-junctions. Synchronized firing of FS neurons is important in the generation of gamma oscillations, at frequencies between 30 and 80 Hz. To understand how these synaptic interactions control synchronization, artificial synaptic conductances were injected in FS cells, and the synaptic phase-resetting function (SPRF), describing how the compound synaptic input perturbs the phase of gamma-frequency spiking as a function of the phase at which it is applied, was measured. GABAergic and gap junctional conductances made distinct contributions to the SPRF, which had a surprisingly simple piecewise linear form, with a sharp midcycle break between phase delay and advance. Analysis of the SPRF showed how the intrinsic biophysical properties of FS neurons and their interconnections allow entrainment of firing over a wide gamma frequency band, whose upper and lower frequency limits are controlled by electrical synapses and GABAergic inhibition respectively.

Highlights

Rhythmic oscillations of concerted electrical activity can occur in the neocortex and hippocampus at gamma frequencies (30– 80 Hz), and are thought to be associated with a variety of cognitive tasks including sensory processing, motor control, and feature binding [1,2]
FS cells are highly interconnected by both gap junctions and chemical inhibition
This model gives us deeper insight into how the FS cells synchronize so effectively at gamma oscillations, and will be a building-block in largescale simulations of the FS cell network aimed at understanding the onset and stability of patterns of gamma oscillation in the cortex

Summary

Introduction

Rhythmic oscillations of concerted electrical activity can occur in the neocortex and hippocampus at gamma frequencies (30– 80 Hz), and are thought to be associated with a variety of cognitive tasks including sensory processing, motor control, and feature binding [1,2]. Synchronous gamma oscillations may be highly localized or widely distributed, even between hemispheres, with or without phase lags between different areas and layers [1]. It appears, that local neocortical circuits have an intrinsic capability for generating gamma oscillations, while sensory inputs and connections from other brain regions may shape the complex spatial patterns of oscillatory interaction. During spontaneous network activity of the neocortex in vivo, the power of intracellular voltage fluctuations at frequencies higher than 10 Hz is dominated by inhibitory postsynaptic potentials, which are correlated with the extracellular gamma rhythm, and which synchronously inhibit nearby pyramidal cells [7]. In the hippocampus and cortex, models of interneuron activity suggest that network oscillations depend on mutually inhibitory synaptic conductances [9,10,11]

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