Abstract
Animals exhibit behavioral and neural responses that persist on longer timescales than transient or fluctuating stimulus inputs. Here, we report that Caenorhabditis elegans uses feedback from the motor circuit to a sensory processing interneuron to sustain its motor state during thermotactic navigation. By imaging circuit activity in behaving animals, we show that a principal postsynaptic partner of the AFD thermosensory neuron, the AIY interneuron, encodes both temperature and motor state information. By optogenetic and genetic manipulation of this circuit, we demonstrate that the motor state representation in AIY is a corollary discharge signal. RIM, an interneuron that is connected with premotor interneurons, is required for this corollary discharge. Ablation of RIM eliminates the motor representation in AIY, allows thermosensory representations to reach downstream premotor interneurons, and reduces the animal's ability to sustain forward movements during thermotaxis. We propose that feedback from the motor circuit to the sensory processing circuit underlies a positive feedback mechanism to generate persistent neural activity and sustained behavioral patterns in a sensorimotor transformation.
Highlights
Animals are able to generate behaviors that persist beyond the timescales of the inciting sensory stimuli
While recurrent connections are abundant in the brain, establishing causality between recurrent circuitry, persistent neural activity, and sustained behavior states has been challenging in part due to the technical difficulties in experimentally dissecting neural dynamics across entire sensorimotor pathways
We have uncovered a role for corollary discharge (CD), a feedback signal from the motor circuit, in sustaining a neural state for forward locomotion during C. elegans thermotaxis
Summary
Animals are able to generate behaviors that persist beyond the timescales of the inciting sensory stimuli. Lasting behavioral states require circuit mechanisms to turn a transient stimulus into persistent neuronal activity (Lee and Dan, 2012; Major and Tank, 2004; Hoopfer et al, 2015; Inagaki et al, 2019; Kennedy et al, 2020). Theoretical studies have explored roles for recurrent circuitry, in particular positive feedback, in generating persistent neural activity (Seung, 1996). While recurrent connections are abundant in the brain, establishing causality between recurrent circuitry, persistent neural activity, and sustained behavior states has been challenging in part due to the technical difficulties in experimentally dissecting neural dynamics across entire sensorimotor pathways
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