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 media...

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Autores principales:	Edgar Buhl, Benjamin Kottler, James J. L. Hodge, Frank Hirth
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/0aaea794aeb948d5b26e08e59be028b0
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spelling	oai:doaj.org-article:0aaea794aeb948d5b26e08e59be028b02021-12-02T15:13:06ZThermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila10.1038/s41598-020-80103-92045-2322https://doaj.org/article/0aaea794aeb948d5b26e08e59be028b02021-01-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-80103-9https://doaj.org/toc/2045-2322Abstract 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, shibire TS , 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.Edgar BuhlBenjamin KottlerJames J. L. HodgeFrank HirthNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-17 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Edgar Buhl Benjamin Kottler James J. L. Hodge Frank Hirth Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
description	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, shibire TS , 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.
format	article
author	Edgar Buhl Benjamin Kottler James J. L. Hodge Frank Hirth
author_facet	Edgar Buhl Benjamin Kottler James J. L. Hodge Frank Hirth
author_sort	Edgar Buhl
title	Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
title_short	Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
title_full	Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
title_fullStr	Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
title_full_unstemmed	Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
title_sort	thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of drosophila
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/0aaea794aeb948d5b26e08e59be028b0
work_keys_str_mv	AT edgarbuhl thermoresponsivemotorbehaviorismediatedbyringneuroncircuitsinthecentralcomplexofdrosophila AT benjaminkottler thermoresponsivemotorbehaviorismediatedbyringneuroncircuitsinthecentralcomplexofdrosophila AT jamesjlhodge thermoresponsivemotorbehaviorismediatedbyringneuroncircuitsinthecentralcomplexofdrosophila AT frankhirth thermoresponsivemotorbehaviorismediatedbyringneuroncircuitsinthecentralcomplexofdrosophila
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Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila

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