Abstract
A fundamental question in neuroscience is whether neuronal circuits with variable circuit parameters that produce similar outputs respond comparably to equivalent perturbations.1–4 Work on the pyloric rhythm of the crustacean stomatogastric ganglion (STG) showed that highly variable sets of intrinsic and synaptic conductances can generate similar circuit activity patterns.5–9 Importantly, in response to physiologically relevant perturbations, these disparate circuit solutions can respond robustly and reliably,10–12 but when exposed to extreme perturbations the underlying circuit parameter differences produce diverse patterns of disrupted activity.7,12,13 In this example, the pyloric circuit is unchanged; only the conductance values vary. In contrast, the gastric mill rhythm in the STG can be generated by distinct circuits when activated by different modulatory neurons and/or neuropeptides.14–21 Generally, these distinct circuits produce different gastric mill rhythms. However, the rhythms driven by stimulating modulatory commissural neuron 1 (MCN1) and bath-applying CabPK (Cancer borealis pyrokinin) peptide generate comparable output patterns, despite having distinct circuits that use separate cellular and synaptic mechanisms.22–25 Here, we use these two gastric mill circuits to determine whether such circuits respond comparably when challenged with persisting (hormonal: CCAP) or acute (sensory: GPR neuron) metabotropic influences. Surprisingly, the hormone-mediated action separates these two rhythms despite activating the same ionic current in the same circuit neuron during both rhythms, whereas the sensory neuron evokes comparable responses despite acting via different synapses during each rhythm. These results highlight the need for caution when inferring the circuit response to a perturbation when that circuit is not well defined physiologically.
•Distinct stimuli evoke similar gastric mill rhythms with different mechanisms•A sensory input, GPR, elicits the same response from both circuit mechanisms•A hormone, CCAP, evokes different outputs from the two circuit mechanisms•Thus, degenerate circuits respond similarly or differently to the same perturbation
Powell et al. study two forms of the gastric mill rhythm that are activated differently, result from different circuit configurations, but produce similar motor patterns. These “degenerate” circuits were challenged by two perturbations, one of which elicits similar outcomes from the two starting circuits, while the other distinguishes between them.