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

Eduarda Susin and Alain Destexhe

PLOS Computational Biology: 17: e1009416, 2021.

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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 in 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.

Author Summary

In the awake and attentive brain, the activity of neurons is typically asynchronous and irregular. It also occasionally displays oscillations in the Gamma frequency range (30-90 Hz), which are believed to be involved in information processing. Here, we use computational models to investigate how brain circuits generate oscillations in a manner consistent with microelectrode recordings in humans. We then study how these networks respond to external input, comparing asynchronous and oscillatory states. This is tested according to several paradigms, an integrative mode, where slowly varying inputs are progressively integrated, a coincidence detection mode, where brief inputs are processed according to the phase of the oscillations, and a resonance mode where the network is probed with oscillatory inputs. Surprisingly, we find that in all cases, the presence of Gamma oscillations tends to diminish the responsiveness to external inputs, and we found no paradigm by which Gamma oscillations would favor information flow compared to asynchronous states. We discuss possible implications of this responsiveness decrease on information processing and propose new directions for further exploration.
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