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Dual Mechanism for the Emergence of Synchronization in Inhibitory Neural Networks.

ABSTRACT: During cognitive tasks cortical microcircuits synchronize to bind stimuli into unified perception. The emergence of coherent rhythmic activity is thought to be inhibition-driven and stimulation-dependent. However, the exact mechanisms of synchronization remain unknown. Recent optogenetic experiments have identified two neuron sub-types as the likely inhibitory vectors of synchronization. Here, we show that local networks mimicking the soma-targeting properties observed in fast-spiking interneurons and the dendrite-projecting properties observed in somatostatin interneurons synchronize through different mechanisms which may provide adaptive advantages by combining flexibility and robustness. We probed the synchronization phase diagrams of small all-to-all inhibitory networks in-silico as a function of inhibition delay, neurotransmitter kinetics, timings and intensity of stimulation. Inhibition delay is found to induce coherent oscillations over a broader range of experimental conditions than high-frequency entrainment. Inhibition delay boosts network capacity (ln2)^-N-fold by stabilizing locally coherent oscillations. This work may inform novel therapeutic strategies for moderating pathological cortical oscillations.

SUBMITTER: Chauhan AS

PROVIDER: S-EPMC6065321 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Dual Mechanism for the Emergence of Synchronization in Inhibitory Neural Networks.

Chauhan Ashok S AS Taylor Joseph D JD Nogaret Alain A

Scientific reports 20180730 1

During cognitive tasks cortical microcircuits synchronize to bind stimuli into unified perception. The emergence of coherent rhythmic activity is thought to be inhibition-driven and stimulation-dependent. However, the exact mechanisms of synchronization remain unknown. Recent optogenetic experiments have identified two neuron sub-types as the likely inhibitory vectors of synchronization. Here, we show that local networks mimicking the soma-targeting properties observed in fast-spiking interneuro ...[more]

PMID: 30061738

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Project description:We developed a multicellular model characterized by a high degree of heterogeneity to investigate possible mechanisms that underlie circadian network synchronization and rhythmicity in the suprachiasmatic nucleus (SCN). We populated a two-dimensional grid with 400 model neurons coupled via ?-aminobutyric acid (GABA) and vasoactive intestinal polypeptide (VIP) neurotransmitters through a putative Ca(2+) mediated signaling cascade to investigate their roles in gene expression and electrical firing activity of cell populations. As observed experimentally, our model predicted that GABA would affect the amplitude of circadian oscillations but not synchrony among individual oscillators. Our model recapitulated experimental findings of decreased synchrony and average periods, loss of rhythmicity, and reduced circadian amplitudes as VIP signaling was eliminated. In addition, simulated increases of VIP reduced periodicity and synchrony. We therefore postulated a physiological range of VIP within which the system is able to produce sustained and synchronized oscillations. Our model recapitulated experimental findings of diminished amplitudes and periodicity with decreasing intracellular Ca(2+) concentrations, suggesting that such behavior could be due to simultaneous decrease of individual oscillation amplitudes and population synchrony. Simulated increases in Cl(-) levels resulted in increased Cl(-) influx into the cytosol, a decrease of inhibitory postsynaptic currents, and ultimately a shift of GABA-elicited responses from inhibitory to excitatory. The simultaneous reduction of IPSCs and increase in membrane resting potential produced GABA dose-dependent increases in firing rates across the population, as has been observed experimentally. By integrating circadian gene regulation and electrophysiology with intracellular and intercellular signaling, we were able to develop the first (to our knowledge) multicellular model that allows the effects of clock genes, electrical firing, Ca(2+), GABA, and VIP on circadian system behavior to be predicted.

Dataset Information

Dual Mechanism for the Emergence of Synchronization in Inhibitory Neural Networks.

Publications

Dual Mechanism for the Emergence of Synchronization in Inhibitory Neural Networks.

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