Biphasic Internetwork Coordination is Funneled through an Electrical Synapse
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Linked rhythmic behaviors, such as respiration/locomotion or swallowing/chewing often require coordination for proper function. Despite its prevalence, the cellular mechanisms controlling coordination of the underlying neural networks remain undetermined in most systems. We use the stomatogastric nervous system of the crab Cancer borealis to investigate mechanisms of internetwork coordination, due to its small, well characterized feeding-related networks (gastric mill [chewing, ∼0.1 Hz]; pyloric [filtering food, ∼1 Hz]). Here, we investigate coordination between these networks during the Gly 1 -SIFamide (SIF) neuropeptide modulatory state. SIF activates a unique triphasic gastric mill rhythm in which the typically pyloric-only LPG neuron generates dual pyloric-plus gastric mill-timed oscillations. Additionally, the pyloric rhythm exhibits increased cycle frequency during gastric mill rhythm-timed LPG bursts, and decreased cycle frequency during IC, or IC plus LG gastric mill neuron bursts. Hyperpolarizing current injections and photoinactivation of network neurons demonstrate that gastric mill rhythm bursts in IC, but not LG, are responsible for decreasing the pyloric frequency, whereas LPG increases pyloric frequency through its rectified electrical coupling to pyloric pacemaker neurons. Surprisingly, LPG photoinactivation also eliminated slowing of the pyloric rhythm. IC firing frequency and gastric mill burst duration were not altered by LPG photoinactivation, suggesting that IC slows the pyloric rhythm primarily via synaptic inhibition of LPG, which then slows the pyloric pacemakers via electrical coupling. Thus, despite its rectification, an electrical synapse directly conveys endogenous bursting and indirectly funnels neurotransmitter-mediated inhibition to enable one network to alternately increase and decrease the frequency of a related network.
Significance Statement
Related rhythmic behaviors frequently exhibit coordination, yet the cellular mechanisms coordinating the underlying neural networks are not determined in most systems. We investigated coordination between two small, well-characterized crustacean feeding-associated networks during a neuropeptide-elicited modulatory state. We find that a dual fast/slow network neuron directly increases fast network frequency during its slow, intrinsically generated bursts, via electrical coupling to fast network pacemakers, despite rectification favoring the opposite direction. Additionally, the fast network is indirectly slowed during another slow-network phase, via chemical synaptic inhibition funneled through the same electrical synapse. Thus, a rectifying electrical synapse alternately reinforces and diminishes neuropeptide actions, enabling distinct frequencies of a faster network across different phases of a related slower rhythm.
