Divisive gain modulation enables flexible and rapid entrainment in a neocortical microcircuit model.

Andrew J Trevelyan,Christoforos A Papasavvas,Yujiang Wang,Marcus Kaiser

doi:10.1152/jn.00401.2019

Andrew J Trevelyan, Christoforos A Papasavvas + Show 2 more

Open Access

https://doi.org/10.1152/jn.00401.2019

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Abstract

Neocortical circuits exhibit a rich dynamic repertoire, and their ability to achieve entrainment (adjustment of their frequency to match the input frequency) is thought to support many cognitive functions and indicate functional flexibility. Although previous studies have explored the influence of various circuit properties on this phenomenon, the role of divisive gain modulation (or divisive inhibition) is unknown. This gain control mechanism is thought to be delivered mainly by the soma-targeting interneurons in neocortical microcircuits. In this study, we use a neural mass model of the neocortical microcircuit (extended Wilson–Cowan model) featuring both soma-targeting and dendrite-targeting interneuronal subpopulations to investigate the role of divisive gain modulation in entrainment. Our results demonstrate that the presence of divisive inhibition in the microcircuit, as delivered by the soma-targeting interneurons, enables its entrainment to a wider range of input frequencies. Divisive inhibition also promotes a faster entrainment, with the microcircuit needing less time to converge to the fully entrained state. We suggest that divisive inhibition, working alongside subtractive inhibition, allows for more adaptive oscillatory responses in neocortical circuits and, thus, supports healthy brain functioning.NEW & NOTEWORTHY We introduce a computational neocortical microcircuit model that features two inhibitory neural populations, with one providing subtractive and the other divisive inhibition to the excitatory population. We demonstrate that divisive inhibition widens the range of input frequencies to which the microcircuit can become entrained and diminishes the time needed to reach full entrainment. We suggest that divisive inhibition enables more adaptive oscillatory activity, with important implications for both normal and pathological brain function.

Highlights

Neural networks exhibit a diverse dynamic repertoire at macroscopic and microscopic scales (Buzsáki 2006; Wright and Liley 1996)
Gamma-band entrainment is impaired in schizophrenia patients, and this impairment is a potential biomarker for the disorder (Brenner et al 2003; Hamm et al 2015; Krishnan et al 2009)
The time constant was set to ␶ ϭ 0.05. This value was chosen based on the response of the neocortical microcircuit model to an instantaneous input, which has a characteristic half-life t1/2 ϭ 39.8 ms, approximating the re

Summary

INTRODUCTION

Neural networks exhibit a diverse dynamic repertoire at macroscopic and microscopic scales (Buzsáki 2006; Wright and Liley 1996). A crucial property of neural circuits is their ability to adjust their oscillation frequency to match a given stimulation frequency. Divisive inhibition appears to increase the stability of oscillations in recurrent circuits (Chance and Abbott 2000; Papasavvas et al 2015; Vida et al 2006) It is still unknown whether divisive inhibition has any effect on neural entrainment. Computational and theoretical studies on neural entrainment, which typically rely on neural mass models, have provided insights into the underlying mechanisms and testable predictions on the use of periodic stimulation (Herrmann et al 2016; Masuda and Kori 2007; Roberts and Robinson 2012; Spiegler et al 2011; Vierling-Claassen et al 2008). By using the input-output function Fe,i, the neocortical microcircuit is described by the following system of ordinary differential equations:

MATERIALS AND METHODS

E Idend Isoma

RESULTS

DISCUSSION

DISCLOSURES