Integration, coincidence detection and resonance in networks of spiking neurons expressing Gamma oscillations and asynchronous states.

Eduarda Susin,Alain Destexhe,Arvind Kumar

doi:10.1371/journal.pcbi.1009416

Abstract

Gamma oscillations are widely seen in the awake and sleeping cerebral cortex, but the exact role of these oscillations is still debated. Here, we used biophysical models to examine how Gamma oscillations may participate to the processing of afferent stimuli. We constructed conductance-based network models of Gamma oscillations, based on different cell types found in cerebral cortex. The models were adjusted to extracellular unit recordings in humans, where Gamma oscillations always coexist with the asynchronous firing mode. We considered three different mechanisms to generate Gamma, first a mechanism based on the interaction between pyramidal neurons and interneurons (PING), second a mechanism in which Gamma is generated by interneuron networks (ING) and third, a mechanism which relies on Gamma oscillations generated by pacemaker chattering neurons (CHING). We find that all three mechanisms generate features consistent with human recordings, but that the ING mechanism is most consistent with the firing rate change inside Gamma bursts seen in the human data. We next evaluated the responsiveness and resonant properties of these networks, contrasting Gamma oscillations with the asynchronous mode. We find that for both slowly-varying stimuli and precisely-timed stimuli, the responsiveness is generally lower during Gamma compared to asynchronous states, while resonant properties are similar around the Gamma band. We could not find conditions where Gamma oscillations were more responsive. We therefore predict that asynchronous states provide the highest responsiveness to external stimuli, while Gamma oscillations tend to overall diminish responsiveness.

Highlights

Gamma oscillations appear in many brain states and brain regions [1] and are detectable mostly from the local field potential (LFP) as oscillations in the 30–90 Hz frequency range.During sensory responses, oscillations in this frequency range were initially proposed to serve as a mechanism for coordination of neural activity among cells coding for different aspects of the same stimulus [2,3,4,5]
The data was acquired extracellularly in patients suffering of intractable epilepsy, who had multielectrode arrays implanted during therapeutic procedures
We considered here one patient for which the recording was very stable, and in which several periods of wakefulness could be analyzed

Summary

Introduction

Gamma oscillations appear in many brain states and brain regions [1] and are detectable mostly from the local field potential (LFP) as oscillations in the 30–90 Hz frequency range.During sensory responses, oscillations in this frequency range were initially proposed to serve as a mechanism for coordination of neural activity among cells coding for different aspects of the same stimulus [2,3,4,5]. Strengthening of synaptic input due to temporal summation led to the hypothesis that Gamma synchrony was necessary to effectively transmit specific sets of information across cortical networks in the very noisy conditions in which the brain operates. This concept was later expanded by proposing that synchronous Gamma engages inhibition in target networks. Phase-locked inhibition creates strong suppression around the excitatory drive and creates windows of low and high neuronal excitability. Such observations led to hypotheses that Gamma oscillations are important for information processing and coding

Methods

Results

Conclusion