Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila

Abstract

Insects are ectothermal animals that are constrained in their survival and reproduction by external temperature fluctuations which require either active avoidance of or movement towards a given heat source. In Drosophila, different thermoreceptors and neurons have been identified that mediate temperature sensation to maintain the animal’s thermal preference. However, less is known how thermosensory information is integrated to gate thermoresponsive motor behavior. Here we use transsynaptic tracing together with calcium imaging, electrophysiology and thermogenetic manipulations in freely moving Drosophila exposed to elevated temperature and identify different functions of ellipsoid body ring neurons, R1-R4, in thermoresponsive motor behavior. Our results show that warming of the external surroundings elicits calcium influx specifically in R2-R4 but not in R1, which evokes threshold-dependent neural activity in the outer layer ring neurons. In contrast to R2, R3 and R4d neurons, thermogenetic inactivation of R4m and R1 neurons expressing the temperature-sensitive mutant allele of dynamin, shibireTS, results in impaired thermoresponsive motor behavior at elevated 31 °C. trans-Tango mediated transsynaptic tracing together with physiological and behavioral analyses indicate that integrated sensory information of warming is registered by neural activity of R4m as input layer of the ellipsoid body ring neuropil and relayed on to R1 output neurons that gate an adaptive motor response. Together these findings imply that segregated activities of central complex ring neurons mediate sensory-motor transformation of external temperature changes and gate thermoresponsive motor behavior in Drosophila.

Comparative analysis of temperature preference behavior and effects of temperature on daily behavior in 11 Drosophila species

“…The temperature preference behavior is a type of decision-making behavior made by specific brain neurons to stay at or leave from the current temperature regime 46 . In D. melanogaster , manipulating the subsets of dopaminergic neurons has altered the temperature preference behavior 47 . Hence, it is possible that the difference in the effect of antenna ablation between these two species is caused by the difference in the manner of utilizing temperature information from the antenna for the decision-making behavior rather than the difference in the properties of antennae as a temperature sensor.…”

Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae

“…The GABAergic tangential neurons inhibit each other as well as postsynaptic columnar cells in a recurrent network called ring attractor, thereby providing a compass-like representation of head directions in the columns of the central complex (Bockhorst & Homberg, 2015;Turner-Evans et al, 2020). Signaling occurs largely via GABA A receptors but GABA B receptor-mediated inhibition has also been demonstrated (Buhl et al, 2021;Turner-Evans et al, 2020).…”

Comparative analysis of temperature preference behavior and effects of temperature on daily behavior in eleven Drosophila species

“…The temperature preference behavior is a type of decision-making behavior made by specific brain neurons to stay at or leave from the current temperature regime [31]. In D. melanogaster , manipulating the subsets of dopaminergic neurons has altered the temperature preference behavior [32]. Hence, it is possible that the difference in the effect of antenna ablation between these two species is caused by the difference in the manner of utilizing temperature information from the antenna for the decision-making behavior rather than the difference in the properties of antennae as a temperature sensor.…”