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A stochastic model of input effectiveness during irregular gamma rhythms

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Abstract

Gamma-band synchronization has been linked to attention and communication between brain regions, yet the underlying dynamical mechanisms are still unclear. How does the timing and amplitude of inputs to cells that generate an endogenously noisy gamma rhythm affect the network activity and rhythm? How does such ”communication through coherence” (CTC) survive in the face of rhythm and input variability? We present a stochastic modelling approach to this question that yields a very fast computation of the effectiveness of inputs to cells involved in gamma rhythms. Our work is partly motivated by recent optogenetic experiments (Cardin et al. Nature, 459(7247), 663–667 2009) that tested the gamma phase-dependence of network responses by first stabilizing the rhythm with periodic light pulses to the interneurons (I). Our computationally efficient model E-I network of stochastic two-state neurons exhibits finite-size fluctuations. Using the Hilbert transform and Kuramoto index, we study how the stochastic phase of its gamma rhythm is entrained by external pulses. We then compute how this rhythmic inhibition controls the effectiveness of external input onto pyramidal (E) cells, and how variability shapes the window of firing opportunity. For transferring the time variations of an external input to the E cells, we find a tradeoff between the phase selectivity and depth of rate modulation. We also show that the CTC is sensitive to the jitter in the arrival times of spikes to the E cells, and to the degree of I-cell entrainment. We further find that CTC can occur even if the underlying deterministic system does not oscillate; quasicycle-type rhythms induced by the finite-size noise retain the basic CTC properties. Finally a resonance analysis confirms the relative importance of the I cell pacing for rhythm generation. Analysis of whole network behaviour, including computations of synchrony, phase and shifts in excitatory-inhibitory balance, can be further sped up by orders of magnitude using two coupled stochastic differential equations, one for each population. Our work thus yields a fast tool to numerically and analytically investigate CTC in a noisy context. It shows that CTC can be quite vulnerable to rhythm and input variability, which both decrease phase preference.

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Acknowledgments

This work was supported by the Natural Sciences and Engineering Research Council of Canada (AL) and the University of Ottawa Research Chair in Neurophysics (AL). G.N. thanks CIHR (Canadian Institute of Health Research), the Michael Smith Foundations EJLB-Michael Smith Chair program, and the Hope for Depression Research Foundation (HDRF) for support.

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Authors and Affiliations

  1. Physics Department, 150 Louis Pasteur Ottawa, Ottawa, Ontario, K1N 6N5, Canada

    Grégory Dumont & André Longtin

  2. Mind, Brain Imaging and Neuroethics, Royal Ottawa Healthcare, Institute of Mental Health Research, Ottawa, Canada

    Grégory Dumont & Georg Northoff

  3. Center for Neural Dynamics, University of Ottawa, Ottawa, Canada

    Grégory Dumont, Georg Northoff & André Longtin

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  1. Grégory Dumont
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  2. Georg Northoff
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Correspondence to Grégory Dumont.

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Dumont, G., Northoff, G. & Longtin, A. A stochastic model of input effectiveness during irregular gamma rhythms. J Comput Neurosci 40, 85–101 (2016). https://doi.org/10.1007/s10827-015-0583-3

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