Synaptic Strengths Dominate Phasing of Motor Circuit: Intrinsic Conductances of Neuron Types Need Not Vary across Animals

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 multicompartmental 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.