Timing-Dependent Potentiation and Depression of Electrical Synapses Contribute to Network Stability in the Crustacean Cardiac Ganglion

Central pattern generators produce many rhythms necessary for survival (e.g., chewing, breathing, locomotion), and doing so often requires coordination of neurons through electrical synapses. Because even neurons of the same type within a network are often differentially tuned, uniformly applied neuromodulators or toxins can result in uncoordinated activity. In the crab (Cancer borealis) cardiac ganglion, potassium channel blockers and serotonin cause increased depolarization of the five electrically coupled motor neurons as well as loss of the normally completely synchronous activity. Given time, compensation occurs that restores excitability and synchrony. One of the underlying mechanisms of this compensation is an increase in coupling among neurons. However, the salient physiological signal that initiates increased coupling has not been determined. Using male C. borealis, we show that it is the loss of synchronous voltage signals between coupled neurons that is at least partly responsible for plasticity in coupling. Shorter offsets in naturalistic activity across a gap junction enhance coupling, whereas longer delays depress coupling. We also provide evidence on why a desynchronization-specific potentiation or depression of the synapse could ultimately be adaptive through using a hybrid network created by artificially coupling two cardiac ganglia. Specifically, a stray neuron may be brought back in line by increasing coupling if its activity is closer to the remainder of the network. However, if a the activity of a neuron is far outside network parameters, it is detrimental to increase coupling, and therefore depression of the synapse removes a potentially harmful influence on the network.

Automated summary

Central pattern generators are important for generating rhythms necessary for survival. Coordination of neurons through electrical synapses is required, but different tuning of neurons within a network can lead to uncoordinated activity. In the crab cardiac ganglion, loss of synchronous voltage signals between coupled neurons is responsible for plasticity in coupling. Understanding this mechanism can help explain how desynchronization-specific potentiation or depression of synapses is adaptive in a hybrid network.