A model hub-and-spoke circuit defines a role for shunting in sensory processing
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Nonrectifying gap junctions allow inactive neurons to inhibit network activity
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Shunting and lateral facilitation both contribute to nose touch perception
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The hub-and-spoke microcircuit mediates analog coincidence detection
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]. 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.
