RT Journal Article
SR Electronic
T1 Synaptic strengths dominate phasing of motor circuit: Intrinsic conductances of neuron types need not vary across animals
JF eneuro
JO eNeuro
FD Society for Neuroscience
SP ENEURO.0417-18.2019
DO 10.1523/ENEURO.0417-18.2019
A1 Cengiz Günay
A1 Anca Doloc-Mihu
A1 Damon G. Lamb
A1 Ronald L. Calabrese
YR 2019
UL http://www.eneuro.org/content/early/2019/07/03/ENEURO.0417-18.2019.abstract
AB Identified neurons and the networks they compose produce stereotypical, albeit individually unique, activity across members of a species. We propose, for a motor circuit driven by a central pattern generator (CPG), that the uniqueness derives mainly from differences in synaptic strength rather than from differences in intrinsic membrane conductances. We studied a dataset of recordings from six leech (Hirudo sp.) heartbeat control networks, containing complete spiking activity patterns from inhibitory premotor interneurons, motor output spike patterns, and synaptic strength patterns to investigate the source of uniqueness. We used a conductance-based multi-compartmental motor neuron model to construct a bilateral motor circuit model, and controlled it by playing recorded input spike trains from premotor interneurons to generate output inhibitory synaptic patterns similar to experimental measurements. By generating different synaptic conductance parameter sets of this circuit model, we found that relative premotor synaptic strengths impinging onto motor neurons must be different across individuals to produce animal-specific output burst phasing. Obtaining unique outputs from each individual’s circuit model did not require different intrinsic ionic conductance parameters. Furthermore, changing intrinsic conductances failed to compensate for modified synaptic strength patterns. Thus the pattern of synaptic strengths of motor neuron inputs is critical for the phasing of this motor circuit and can explain individual differences. When intrinsic conductances were allowed to vary, they exhibited the same conductance correlations across individuals, suggesting a motor neuron ’type’ required for proper network function. Our results are general and may translate to other systems and neuronal networks that control output phasing.Significance Statement Each member of a species is unique, down to its neurons. The ability to experimentally identify a specific neuron across individuals allows investigating the neuron’s variability in spiking activity patterns and therefore its function. Identified neuron types produce stereotypical, albeit individually unique, activity patterns. Uniqueness of activity can be caused by variability observed in the intrinsic properties of neurons and the synaptic connections of the circuit. Here, we propose that, for a rhythmic neuronal motor circuit, the uniqueness derives mainly from differences in synaptic strength rather than from differences in intrinsic membrane conductances. The neuron types that we studied are from the leech heartbeat system. However, our results are general and can translate to other neuronal networks that control output phasing.