Abstract
SummaryElectrical synapses have been shown to be important for enabling and detecting neuronal synchrony in both vertebrates [1–4] and invertebrates [5, 6]. Hub-and-spoke circuits, in which a central hub neuron is electrically coupled to several input neurons, are an overrepresented motif in the C. elegans nervous system [7] and may represent a conserved functional unit. The functional relevance of this configuration has been demonstrated for circuits mediating aggregation behavior [8] and nose touch perception [9]. Modeling approaches have been useful for understanding structurally and dynamically more complex electrical circuits [10, 11]. Therefore, we formulated a simple analytical model with minimal assumptions to obtain insight into the properties of the hub-and-spoke microcircuit motif. A key prediction of the model is that an active input neuron should facilitate activity throughout the network, whereas an inactive input should suppress network activity through shunting; this prediction was supported by cell ablation and in vivo neuroimaging experiments in the C. elegans nose touch circuit. Thus, the hub-and-spoke architecture may implement an analog coincidence detector enabling distinct responses to distributed and localized patterns of sensory input.
Highlights
Since the time course of sensory inputs is substantially slower than the neurons’ electrical time constants, and since C. elegans neurons are characterized by graded potentials rather than action potentials, we focused on the steady state rather than the dynamics of the circuit, reasoning that we could derive analytical expressions for the membrane potentials in each neuron of the model circuit
We examined the effect of an inactive input on the C. elegans nose touch circuit by either silencing a spoke neuron class or ablating it (Figures 2 and 3)
We showed previously [9] that active mechanoreceptors facilitate the responses of other sensory neurons in the network to low-threshold stimuli through gap-junction-mediated lateral facilitation
Summary
Electrical synapses have been shown to be important for enabling and detecting neuronal synchrony in both vertebrates [1,2,3,4] and invertebrates [5, 6]. Hub-and-spoke circuits, in which a central hub neuron is electrically coupled to several input neurons, are an overrepresented motif in the C. elegans nervous system [7] and may represent a conserved functional unit. The functional relevance of this configuration has been demonstrated for circuits mediating aggregation behavior [8] and nose touch perception [9]. A key prediction of the model is that an active input neuron should facilitate activity throughout the network, whereas an inactive input should suppress network activity through shunting; this prediction was supported by cell ablation and in vivo neuroimaging experiments in the C. elegans nose touch circuit. The hub-and-spoke architecture may implement an analog coincidence detector enabling distinct responses to distributed and localized patterns of sensory input
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