Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior.

Boris P Chagnaud,Paul M Forlano,Jonathan T Perelmuter,Andrew H Bass

doi:10.7554/elife.59390

Boris P Chagnaud, Paul M Forlano + Show 2 more

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https://doi.org/10.7554/elife.59390

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Abstract

Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signaling. Acoustic signaling is an important communication modality for vertebrates, including many teleost fishes. Toadfishes are well known to exhibit high temporal fidelity in synchronous motoneuron firing within a hindbrain network directly determining the temporal structure of natural calls. Here, we investigated how these motoneurons maintain synchronous activation. We show that pronounced temporal precision in population-level motoneuronal firing depends on gap junction-mediated, glycinergic inhibition that generates a period of reduced probability of motoneuron activation. Super-resolution microscopy confirms glycinergic release sites formed by a subset of adjacent premotoneurons contacting motoneuron somata and dendrites. In aggregate, the evidence supports the hypothesis that gap junction-mediated, glycinergic inhibition provides a timing mechanism for achieving synchrony and temporal precision in the millisecond range for rapid modulation of acoustic waveforms.

Highlights

Complex behaviors often depend on temporally precise neuronal firing that coordinates network activity at brain levels ranging from cortical microcircuits to hindbrain pattern generators (Llinas, 2014; Kros et al, 2017; Sober et al, 2018)
These findings strongly suggest that the HYP is mediated by a glycinergic inhibition dependent on gap junctional coupling
Our experiments support the hypothesis that gap junction-mediated activation of glycinergic neurons can account for remarkable synchrony in motoneuron firing and likely contributes to pattern generation

Summary

Introduction

Complex behaviors often depend on temporally precise neuronal firing that coordinates network activity at brain levels ranging from cortical microcircuits to hindbrain pattern generators (Llinas, 2014; Kros et al, 2017; Sober et al, 2018). Mechanisms known to increase precision at single cell and network levels include, for instance, feed-forward inhibition in auditory circuits (Grothe, 2003), recurrent inhibitory input in cerebral cortex (Kapfer et al, 2007), and neuronal synchrony in cortical and sensory neurons (Tiesinga and Sejnowski, 2001; Uhlhaas et al, 2010). Several mechanisms by themselves or in combination contribute to neuronal synchrony: coherent excitatory firing, electrotonic coupling, and inhibitory input (Singer, 1999; Uhlhaas and Singer, 2006; Kapfer et al, 2007). Electrotonic coupling enhances synchrony by spreading voltage changes, for example, during synaptic inputs, that lead to concomitant membrane potential changes within an electrotonic, interconnected population (Bennett and Zukin, 2004; Pereda, 2014)

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