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Electrical Synapse Rectification Enables Dual-Network Activity in the crab Cancer borealis

Savanna-Rae H. Fahoum,F. Nadim,Dawn M. Blitz

Published 2024 in bioRxiv

ABSTRACT

Flexibility of rhythmic networks includes neuromodulator-elicited changes in neuronal participation between networks. We are examining the role of rectifying electrical synapses in this neuronal switching. Electrical synapses can have complex, non-intuitive effects on network output. However, it is often difficult to measure and manipulate rectification across conditions to determine their functional contributions. Here, we use the Jonah crab Cancer borealis to investigate rectification in well-described rhythmic networks. In an established modulatory state, stimulating the projection neuron MCN5 or bath applying its neuropeptide Gly1-SIFamide causes the two LPG neurons to switch from pyloric rhythm-only (food filtering, ∼1 Hz) activity to dual pyloric and gastric mill rhythm (chewing, ∼0.1 Hz) activity. Typically, LPG is co-active with the two PD and single AB pyloric pacemaker neurons due to rectifying electrical coupling. In Gly1-SIFamide, LPG continues to burst in pyloric time with AB/PD but periodically “escapes” and generates intrinsic longer-duration gastric mill-timed bursts, decreasing its overall synchrony with AB/PD, while AB/PD retain their synchronous pyloric timing. Using two-electrode voltage clamp recordings, we find that Gly1-SIFamide does not alter electrical coupling strength or the rectification between LPG and AB/PD. However, in a computational model, rectification is necessary for LPG to escape AB/PD electrical coupling and generate longer, gastric mill-timed bursts. This was confirmed in the biological system by adding a dynamic clamp non-rectifying electrical synapse between LPG and PD, which decreased LPG’s escape from AB/PD and its gastric mill-timed activity. Thus, rectification between electrically coupled oscillators can underlie modulator-elicited changes in their synchrony. Significance statement Behavioral adaptability includes rapid changes in neural circuit composition. Unlike chemical synapses, little is known about electrical synapse contributions to circuit flexibility. Here, we identify an important role for electrical coupling rectification (asymmetrical current flow between coupled neurons) in regulating neuronal participation between neural circuits. A neuromodulator causes the activity of two sets of electrically-coupled neurons participating in an oscillatory neural circuit to diverge, allowing one set to additionally participate in a second oscillatory circuit at a distinct frequency. Using mathematical modeling and the dynamic clamp technique, we show that this transition depends on rectification. This newly-identified function of electrical synapse rectification may have implications for oscillatory networks underlying a range of functions, due to the prevalence of electrical coupling.

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