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Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters

BACKGROUND: Circadian disruptions through frequent transmeridian travel, rotating shift work, and poor sleep hygiene are associated with an array of physical and mental health maladies, including marked deficits in human cognitive function. Despite anecdotal and correlational reports suggesting a ne...

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Autores principales: Gibson, Erin M., Wang, Connie, Tjho, Stephanie, Khattar, Neera, Kriegsfeld, Lance J.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2995744/
https://www.ncbi.nlm.nih.gov/pubmed/21152025
http://dx.doi.org/10.1371/journal.pone.0015267
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author Gibson, Erin M.
Wang, Connie
Tjho, Stephanie
Khattar, Neera
Kriegsfeld, Lance J.
author_facet Gibson, Erin M.
Wang, Connie
Tjho, Stephanie
Khattar, Neera
Kriegsfeld, Lance J.
author_sort Gibson, Erin M.
collection PubMed
description BACKGROUND: Circadian disruptions through frequent transmeridian travel, rotating shift work, and poor sleep hygiene are associated with an array of physical and mental health maladies, including marked deficits in human cognitive function. Despite anecdotal and correlational reports suggesting a negative impact of circadian disruptions on brain function, this possibility has not been experimentally examined. METHODOLOGY/PRINCIPAL FINDINGS: In the present study, we investigated whether experimental ‘jet lag’ (i.e., phase advances of the light∶dark cycle) negatively impacts learning and memory and whether any deficits observed are associated with reductions in hippocampal cell proliferation and neurogenesis. Because insults to circadian timing alter circulating glucocorticoid and sex steroid concentrations, both of which influence neurogenesis and learning/memory, we assessed the contribution of these endocrine factors to any observed alterations. Circadian disruption resulted in pronounced deficits in learning and memory paralleled by marked reductions in hippocampal cell proliferation and neurogenesis. Significantly, deficits in hippocampal-dependent learning and memory were not only seen during the period of the circadian disruption, but also persisted well after the cessation of jet lag, suggesting long-lasting negative consequences on brain function. CONCLUSIONS/SIGNIFICANCE: Together, these findings support the view that circadian disruptions suppress hippocampal neurogenesis via a glucocorticoid-independent mechanism, imposing pronounced and persistent impairments on learning and memory.
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spelling pubmed-29957442010-12-10 Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters Gibson, Erin M. Wang, Connie Tjho, Stephanie Khattar, Neera Kriegsfeld, Lance J. PLoS One Research Article BACKGROUND: Circadian disruptions through frequent transmeridian travel, rotating shift work, and poor sleep hygiene are associated with an array of physical and mental health maladies, including marked deficits in human cognitive function. Despite anecdotal and correlational reports suggesting a negative impact of circadian disruptions on brain function, this possibility has not been experimentally examined. METHODOLOGY/PRINCIPAL FINDINGS: In the present study, we investigated whether experimental ‘jet lag’ (i.e., phase advances of the light∶dark cycle) negatively impacts learning and memory and whether any deficits observed are associated with reductions in hippocampal cell proliferation and neurogenesis. Because insults to circadian timing alter circulating glucocorticoid and sex steroid concentrations, both of which influence neurogenesis and learning/memory, we assessed the contribution of these endocrine factors to any observed alterations. Circadian disruption resulted in pronounced deficits in learning and memory paralleled by marked reductions in hippocampal cell proliferation and neurogenesis. Significantly, deficits in hippocampal-dependent learning and memory were not only seen during the period of the circadian disruption, but also persisted well after the cessation of jet lag, suggesting long-lasting negative consequences on brain function. CONCLUSIONS/SIGNIFICANCE: Together, these findings support the view that circadian disruptions suppress hippocampal neurogenesis via a glucocorticoid-independent mechanism, imposing pronounced and persistent impairments on learning and memory. Public Library of Science 2010-12-01 /pmc/articles/PMC2995744/ /pubmed/21152025 http://dx.doi.org/10.1371/journal.pone.0015267 Text en Gibson et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Gibson, Erin M.
Wang, Connie
Tjho, Stephanie
Khattar, Neera
Kriegsfeld, Lance J.
Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters
title Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters
title_full Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters
title_fullStr Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters
title_full_unstemmed Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters
title_short Experimental ‘Jet Lag’ Inhibits Adult Neurogenesis and Produces Long-Term Cognitive Deficits in Female Hamsters
title_sort experimental ‘jet lag’ inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2995744/
https://www.ncbi.nlm.nih.gov/pubmed/21152025
http://dx.doi.org/10.1371/journal.pone.0015267
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