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Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging

Sensory perception modulates aging, yet we know little about how. An understanding of the neuronal mechanisms through which animals orchestrate biological responses to relevant sensory inputs would provide insight into the control systems that may be important for modulating lifespan. Here, we provi...

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Autores principales: Gendron, Christi M., Chakraborty, Tuhin S., Duran, Cathryn, Dono, Thomas, Pletcher, Scott D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10263353/
https://www.ncbi.nlm.nih.gov/pubmed/37310911
http://dx.doi.org/10.1371/journal.pbio.3002149
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author Gendron, Christi M.
Chakraborty, Tuhin S.
Duran, Cathryn
Dono, Thomas
Pletcher, Scott D.
author_facet Gendron, Christi M.
Chakraborty, Tuhin S.
Duran, Cathryn
Dono, Thomas
Pletcher, Scott D.
author_sort Gendron, Christi M.
collection PubMed
description Sensory perception modulates aging, yet we know little about how. An understanding of the neuronal mechanisms through which animals orchestrate biological responses to relevant sensory inputs would provide insight into the control systems that may be important for modulating lifespan. Here, we provide new awareness into how the perception of dead conspecifics, or death perception, which elicits behavioral and physiological effects in many different species, affects lifespan in the fruit fly, Drosophila melanogaster. Previous work demonstrated that cohousing Drosophila with dead conspecifics decreases fat stores, reduces starvation resistance, and accelerates aging in a manner that requires both sight and the serotonin receptor 5-HT2A. In this manuscript, we demonstrate that a discrete, 5-HT2A-expressing neural population in the ellipsoid body (EB) of the Drosophila central complex, identified as R2/R4 neurons, acts as a rheostat and plays an important role in transducing sensory information about the presence of dead individuals to modulate lifespan. Expression of the insulin-responsive transcription factor foxo in R2/R4 neurons and insulin-like peptides dilp3 and dilp5, but not dilp2, are required, with the latter likely altered in median neurosecretory cells (MNCs) after R2/R4 neuronal activation. These data generate new insights into the neural underpinnings of how perceptive events may impact aging and physiology across taxa.
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spelling pubmed-102633532023-06-15 Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging Gendron, Christi M. Chakraborty, Tuhin S. Duran, Cathryn Dono, Thomas Pletcher, Scott D. PLoS Biol Short Reports Sensory perception modulates aging, yet we know little about how. An understanding of the neuronal mechanisms through which animals orchestrate biological responses to relevant sensory inputs would provide insight into the control systems that may be important for modulating lifespan. Here, we provide new awareness into how the perception of dead conspecifics, or death perception, which elicits behavioral and physiological effects in many different species, affects lifespan in the fruit fly, Drosophila melanogaster. Previous work demonstrated that cohousing Drosophila with dead conspecifics decreases fat stores, reduces starvation resistance, and accelerates aging in a manner that requires both sight and the serotonin receptor 5-HT2A. In this manuscript, we demonstrate that a discrete, 5-HT2A-expressing neural population in the ellipsoid body (EB) of the Drosophila central complex, identified as R2/R4 neurons, acts as a rheostat and plays an important role in transducing sensory information about the presence of dead individuals to modulate lifespan. Expression of the insulin-responsive transcription factor foxo in R2/R4 neurons and insulin-like peptides dilp3 and dilp5, but not dilp2, are required, with the latter likely altered in median neurosecretory cells (MNCs) after R2/R4 neuronal activation. These data generate new insights into the neural underpinnings of how perceptive events may impact aging and physiology across taxa. Public Library of Science 2023-06-13 /pmc/articles/PMC10263353/ /pubmed/37310911 http://dx.doi.org/10.1371/journal.pbio.3002149 Text en © 2023 Gendron et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Short Reports
Gendron, Christi M.
Chakraborty, Tuhin S.
Duran, Cathryn
Dono, Thomas
Pletcher, Scott D.
Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging
title Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging
title_full Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging
title_fullStr Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging
title_full_unstemmed Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging
title_short Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging
title_sort ring neurons in the drosophila central complex act as a rheostat for sensory modulation of aging
topic Short Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10263353/
https://www.ncbi.nlm.nih.gov/pubmed/37310911
http://dx.doi.org/10.1371/journal.pbio.3002149
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