Tyraminergic corollary discharge filters reafferent perception in a chemosensory neuron

Julia Riedl; Charles Fieseler; Manuel Zimmer

doi:10.1016/j.cub.2022.05.051

Tyraminergic corollary discharge filters reafferent perception in a chemosensory neuron

Department für Neurowissenschaften und Entwicklungsbiologie

Veröffentlichungen: Beitrag in Fachzeitschrift › Artikel › Peer Reviewed

Abstract

nterpreting sensory information requires its integration with the current behavior of the animal. However, how motor-related circuits influence sensory information processing is incompletely understood. Here, we report that current locomotor state directly modulates the activity of BAG CO2 sensory neurons in Caenorhabditis elegans. By recording neuronal activity in animals freely navigating CO2 landscapes, we found that during reverse crawling states, BAG activity is suppressed by tyraminergic corollary discharge signaling. We provide genetic evidence that tyramine released from the RIM reversal interneurons extrasynaptically activates the inhibitory chloride channel LGC-55 in BAG. Disrupting this pathway genetically leads to excessive behavioral responses to CO2 stimuli. Moreover, we find that LGC-55 signaling cancels out perception of self-produced CO2 and O2 stimuli when animals reverse into their own gas plume in ethologically relevant aqueous environments. Our results show that sensorimotor integration involves corollary discharge signals directly modulating chemosensory neurons.

Originalsprache	Englisch
Aufsatznummer	e6
Seiten (von - bis)	3048-3058
Seitenumfang	18
Fachzeitschrift	Current Biology
Jahrgang	32
Ausgabenummer	14
DOIs	https://doi.org/10.1016/j.cub.2022.05.051
Publikationsstatus	Veröffentlicht - 25 Juli 2022

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We thank Mark Alkema for plasmids; Cornelia Bargmann for strains; the Luisa Cochella lab for plasmids, strains, and technical support; and Ilona G. Kadow, Harris Kaplan, and the Zimmer lab for critical feedback and support. The research leading to these results has received funding from the Simons Foundation (# 324958 ), the University of Vienna , and the Research Institute of Molecular Pathology (IMP). C.F. is supported by a VIP2 postdoctoral fellowship co-funded by the European Union\u2019s Horizon 2020 research and innovation program under the Marie Sk\u0142odowska-Curie grant agreement no. 847548 . M.Z. is supported by the Simons Foundation (# 543069 ) and the International Research Scholar Program by the Wellcome Trust and Howard Hughes Medical Institute (# 208565/A/17/Z ). The IMP is funded by Boehringer Ingelheim . We thank Mark Alkema for plasmids; Cornelia Bargmann for strains; the Luisa Cochella lab for plasmids, strains, and technical support; and Ilona G. Kadow, Harris Kaplan, and the Zimmer lab for critical feedback and support. The research leading to these results has received funding from the Simons Foundation (#324958), the University of Vienna, and the Research Institute of Molecular Pathology (IMP). C.F. is supported by a VIP2 postdoctoral fellowship co-funded by the European Union's Horizon 2020 research and innovation program under the Marie Sk\u0142odowska-Curie grant agreement no. 847548. M.Z. is supported by the Simons Foundation (#543069) and the International Research Scholar Program by the Wellcome Trust and Howard Hughes Medical Institute (#208565/A/17/Z). The IMP is funded by Boehringer Ingelheim. J.R. designed and performed experiments, developed analytical methods, analyzed data, and wrote the manuscript. C.F. designed and performed CO2 diffusion simulations. M.Z. led the project and wrote the manuscript. The authors declare no competing interests.

ÖFOS 2012

106023 Molekularbiologie
106025 Neurobiologie

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10.1016/j.cub.2022.05.051Lizenz: CC BY 4.0

https://phaidra.univie.ac.at/o:1634805Lizenz: CC BY 4.0

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abstract = "nterpreting sensory information requires its integration with the current behavior of the animal. However, how motor-related circuits influence sensory information processing is incompletely understood. Here, we report that current locomotor state directly modulates the activity of BAG CO2 sensory neurons in Caenorhabditis elegans. By recording neuronal activity in animals freely navigating CO2 landscapes, we found that during reverse crawling states, BAG activity is suppressed by tyraminergic corollary discharge signaling. We provide genetic evidence that tyramine released from the RIM reversal interneurons extrasynaptically activates the inhibitory chloride channel LGC-55 in BAG. Disrupting this pathway genetically leads to excessive behavioral responses to CO2 stimuli. Moreover, we find that LGC-55 signaling cancels out perception of self-produced CO2 and O2 stimuli when animals reverse into their own gas plume in ethologically relevant aqueous environments. Our results show that sensorimotor integration involves corollary discharge signals directly modulating chemosensory neurons.",

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N2 - nterpreting sensory information requires its integration with the current behavior of the animal. However, how motor-related circuits influence sensory information processing is incompletely understood. Here, we report that current locomotor state directly modulates the activity of BAG CO2 sensory neurons in Caenorhabditis elegans. By recording neuronal activity in animals freely navigating CO2 landscapes, we found that during reverse crawling states, BAG activity is suppressed by tyraminergic corollary discharge signaling. We provide genetic evidence that tyramine released from the RIM reversal interneurons extrasynaptically activates the inhibitory chloride channel LGC-55 in BAG. Disrupting this pathway genetically leads to excessive behavioral responses to CO2 stimuli. Moreover, we find that LGC-55 signaling cancels out perception of self-produced CO2 and O2 stimuli when animals reverse into their own gas plume in ethologically relevant aqueous environments. Our results show that sensorimotor integration involves corollary discharge signals directly modulating chemosensory neurons.

AB - nterpreting sensory information requires its integration with the current behavior of the animal. However, how motor-related circuits influence sensory information processing is incompletely understood. Here, we report that current locomotor state directly modulates the activity of BAG CO2 sensory neurons in Caenorhabditis elegans. By recording neuronal activity in animals freely navigating CO2 landscapes, we found that during reverse crawling states, BAG activity is suppressed by tyraminergic corollary discharge signaling. We provide genetic evidence that tyramine released from the RIM reversal interneurons extrasynaptically activates the inhibitory chloride channel LGC-55 in BAG. Disrupting this pathway genetically leads to excessive behavioral responses to CO2 stimuli. Moreover, we find that LGC-55 signaling cancels out perception of self-produced CO2 and O2 stimuli when animals reverse into their own gas plume in ethologically relevant aqueous environments. Our results show that sensorimotor integration involves corollary discharge signals directly modulating chemosensory neurons.

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Tyraminergic corollary discharge filters reafferent perception in a chemosensory neuron

Abstract

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ÖFOS 2012

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