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Research Articles, Systems/Circuits

Microcircuit Synchronization and Heavy-Tailed Synaptic Weight Distribution Augment preBötzinger Complex Bursting Dynamics

Sufyan Ashhad, Valentin M. Slepukhin, Jack L. Feldman and Alex J. Levine
Journal of Neuroscience 11 January 2023, 43 (2) 240-260; DOI: https://doi.org/10.1523/JNEUROSCI.1195-22.2022
Sufyan Ashhad
1Department of Neurobiology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 90095-1763
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Valentin M. Slepukhin
2Department of Physics & Astronomy, University of California, Los Angeles, Los Angeles, California 90095-1596
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Jack L. Feldman
1Department of Neurobiology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 90095-1763
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Alex J. Levine
2Department of Physics & Astronomy, University of California, Los Angeles, Los Angeles, California 90095-1596
3Department of Chemistry & Biochemistry, University of California, Los Angeles, Los Angeles, California 90095-1596
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Abstract

The preBötzinger Complex (preBötC) encodes inspiratory time as rhythmic bursts of activity underlying each breath. Spike synchronization throughout a sparsely connected preBötC microcircuit initiates bursts that ultimately drive the inspiratory motor patterns. Using minimal microcircuit models to explore burst initiation dynamics, we examined the variability in probability and latency to burst following exogenous stimulation of a small subset of neurons, mimicking experiments. Among various physiologically plausible graphs of 1000 excitatory neurons constructed using experimentally determined synaptic and connectivity parameters, directed Erdős-Rényi graphs with a broad (lognormal) distribution of synaptic weights best captured the experimentally observed dynamics. preBötC synchronization leading to bursts was regulated by the efferent connectivity of spiking neurons that are optimally tuned to amplify modest preinspiratory activity through input convergence. Using graph-theoretic and machine learning-based analyses, we found that input convergence of efferent connectivity at the next-nearest neighbor order was a strong predictor of incipient synchronization. Our analyses revealed a crucial role of synaptic heterogeneity in imparting exceptionally robust yet flexible preBötC attractor dynamics. Given the pervasiveness of lognormally distributed synaptic strengths throughout the nervous system, we postulate that these mechanisms represent a ubiquitous template for temporal processing and decision-making computational motifs.

SIGNIFICANCE STATEMENT Mammalian breathing is robust, virtually continuous throughout life, yet is inherently labile: to adapt to rapid metabolic shifts (e.g., fleeing a predator or chasing prey); for airway reflexes; and to enable nonventilatory behaviors (e.g., vocalization, breathholding, laughing). Canonical theoretical frameworks—based on pacemakers and intrinsic bursting—cannot account for the observed robustness and flexibility of the preBötzinger Complex rhythm. Experiments reveal that network synchronization is the key to initiate inspiratory bursts in each breathing cycle. We investigated preBötC synchronization dynamics using network models constructed with experimentally determined neuronal and synaptic parameters. We discovered that a fat-tailed (non-Gaussian) synaptic weight distribution—a manifestation of synaptic heterogeneity—augments neuronal synchronization and attractor dynamics in this vital rhythmogenic network, contributing to its extraordinary reliability and responsiveness.

  • attractor dynamics
  • breathing rhythm
  • graph neural network
  • motor systems
  • preBötzinger Complex
  • synchronization

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The Journal of Neuroscience: 43 (2)
Journal of Neuroscience
Vol. 43, Issue 2
11 Jan 2023
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Microcircuit Synchronization and Heavy-Tailed Synaptic Weight Distribution Augment preBötzinger Complex Bursting Dynamics
Sufyan Ashhad, Valentin M. Slepukhin, Jack L. Feldman, Alex J. Levine
Journal of Neuroscience 11 January 2023, 43 (2) 240-260; DOI: 10.1523/JNEUROSCI.1195-22.2022

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Microcircuit Synchronization and Heavy-Tailed Synaptic Weight Distribution Augment preBötzinger Complex Bursting Dynamics
Sufyan Ashhad, Valentin M. Slepukhin, Jack L. Feldman, Alex J. Levine
Journal of Neuroscience 11 January 2023, 43 (2) 240-260; DOI: 10.1523/JNEUROSCI.1195-22.2022
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Keywords

  • attractor dynamics
  • breathing rhythm
  • graph neural network
  • motor systems
  • preBötzinger Complex
  • synchronization

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