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Specific configurations of electrical synapses filter sensory information to drive choices in behavior

Agustin Almoril-PorrasiD, Ana C. Calvo, Longgang NiuiD, Jonathan A. BeaganiD, Joshua D. HawkiD, Ahmad Z. AljobehiD, Elias M. WisdomiD, Ivy ReniD, Malcom Díaz GarcíaiD, Zhao‐Wen WangiD, Daniel A. Colón‐RamosiD

Abstract

Synaptic configurations in precisely wired circuits underpin how sensory information is processed by the nervous system, and the emerging animal behavior. This is best understood for chemical synapses, but far less is known about how electrical synaptic configurations modulate, in vivo and in specific neurons, sensory information processing and context-specific behaviors. We discovered that INX-1, a gap junction protein that forms electrical synapses, is required to deploy context-specific behavioral strategies during C. elegans thermotaxis behavior. INX-1 couples two bilaterally symmetric interneurons, and this configuration is required for the integration of sensory information during migration of animals across temperature gradients. In inx-1 mutants, uncoupled interneurons display increased excitability and responses to subthreshold temperature stimuli, resulting in abnormally longer run durations and context-irrelevant tracking of isotherms. Our study uncovers a conserved configuration of electrical synapses that, by increasing neuronal capacitance, enables differential processing of sensory information and the deployment of context-specific behavioral strategies. One-Sentence SummaryCoupling of interneurons by electrical synapses reduces membrane resistance and filters sensory inputs to guide sensory-dependent behavioral choices.

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