Multiple Muscles Respond Differently to the Same Dual-Network Motor Neuron Activity

Coordination between central pattern generator (CPG) networks underlies coordination of related rhythmic behaviors (e.g., mastication, respiration). This includes individual neurons periodically expressing activity related to more than one behavior. Here, we investigated whether muscles involved in different behaviors respond broadly to dual-network activity, or are biased toward their primary network input. We used the pyloric ("fast": ∼1 Hz: filtering of food) and gastric mill ("slow": ∼0.1 Hz: chewing) networks in the crab, Cancer borealis. During the modulatory state elicited by the neuropeptide Gly¹-SIFamide, the pyloric-only lateral posterior gastric (LPG) neuron switches to dual pyloric and gastric mill network participation, enabling its contributions to inter-network coordination. LPG innervates pyloric (p7) and gastric mill (gm3b,c) muscles. Using intracellular muscle fiber recordings, we found that p7 responded to single LPG stimuli whereas gm3 required bursts to generate measurable responses. Naturalistic or fixed-parameter dual-network stimulations elicited similar peak p7 amplitudes for both network components. In contrast, gm3 primarily responded to longer-duration, slower-frequency gastric mill bursts. There were reciprocal interactions between the p7 pyloric and gastric mill responses, whereas it was unidirectional in gm3. The inter-network influences in p7 are likely due to activity-dependent synaptic plasticity which we found occurring at multiple time scales, but this was difficult to assess in gm3. Thus, interactions at the motor network level can be translated to electrical responses of muscles. However, the activity of some, but not all, muscles may be tuned to a primary behavior, even for muscles innervated by the same motor neuron.