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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Main Authors: Christi M Gendron, Tuhin S Chakraborty, Cathryn Duran, Thomas Dono, Scott D Pletcher
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-06-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002149
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author Christi M Gendron
Tuhin S Chakraborty
Cathryn Duran
Thomas Dono
Scott D Pletcher
author_facet Christi M Gendron
Tuhin S Chakraborty
Cathryn Duran
Thomas Dono
Scott D Pletcher
author_sort Christi M Gendron
collection DOAJ
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 doaj-art-3660b299f5aa4a66b098a95d82d6be5b2025-08-20T03:54:07ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-06-01216e300214910.1371/journal.pbio.3002149Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging.Christi M GendronTuhin S ChakrabortyCathryn DuranThomas DonoScott D PletcherSensory 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.https://doi.org/10.1371/journal.pbio.3002149
spellingShingle Christi M Gendron
Tuhin S Chakraborty
Cathryn Duran
Thomas Dono
Scott D Pletcher
Ring neurons in the Drosophila central complex act as a rheostat for sensory modulation of aging.
PLoS Biology
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
url https://doi.org/10.1371/journal.pbio.3002149
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