Cargando…

Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats

Adult neurogenesis modifies hippocampal circuits and behavior, but removing newborn neurons does not consistently alter spatial processing, a core function of the hippocampus. Additionally, little is known about sex differences in neurogenesis since few studies have compared males and females. Since...

Descripción completa

Detalles Bibliográficos
Autores principales: O’Leary, Timothy P., Askari, Baran, Lee, Bonnie H., Darby, Kathryn, Knudson, Cypress, Ash, Alyssa M., Seib, Desiree R., Espinueva, Delane F., Snyder, Jason S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9116935/
https://www.ncbi.nlm.nih.gov/pubmed/35473765
http://dx.doi.org/10.1523/ENEURO.0054-22.2022
_version_ 1784710218524917760
author O’Leary, Timothy P.
Askari, Baran
Lee, Bonnie H.
Darby, Kathryn
Knudson, Cypress
Ash, Alyssa M.
Seib, Desiree R.
Espinueva, Delane F.
Snyder, Jason S.
author_facet O’Leary, Timothy P.
Askari, Baran
Lee, Bonnie H.
Darby, Kathryn
Knudson, Cypress
Ash, Alyssa M.
Seib, Desiree R.
Espinueva, Delane F.
Snyder, Jason S.
author_sort O’Leary, Timothy P.
collection PubMed
description Adult neurogenesis modifies hippocampal circuits and behavior, but removing newborn neurons does not consistently alter spatial processing, a core function of the hippocampus. Additionally, little is known about sex differences in neurogenesis since few studies have compared males and females. Since adult-born neurons regulate the stress response, we hypothesized that spatial functions may be more prominent under aversive conditions and may differ between males and females given sex differences in stress responding. We therefore trained intact and neurogenesis-deficient rats in the spatial water maze at temperatures that vary in their degree of aversiveness. In the standard water maze, ablating neurogenesis did not alter spatial learning in either sex. However, in cold water, ablating neurogenesis had divergent sex-dependent effects: relative to intact rats, male neurogenesis-deficient rats were slower to escape the maze and female neurogenesis-deficient rats were faster. Neurogenesis promoted temperature-related changes in search strategy in females, but it promoted search strategy stability in males. Females displayed greater recruitment (Fos expression) of the dorsal hippocampus than males, particularly in cold water. However, blocking neurogenesis did not alter Fos expression in either sex. Finally, morphologic analyses revealed greater experience-dependent plasticity in males. Adult-born neurons in males and females had similar morphology at baseline but training increased spine density and reduced presynaptic terminal size, specifically in males. Collectively, these findings indicate that adult-born neurons contribute to spatial learning in stressful conditions and they provide new evidence for sex differences in their behavioral functions.
format Online
Article
Text
id pubmed-9116935
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Society for Neuroscience
record_format MEDLINE/PubMed
spelling pubmed-91169352022-05-19 Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats O’Leary, Timothy P. Askari, Baran Lee, Bonnie H. Darby, Kathryn Knudson, Cypress Ash, Alyssa M. Seib, Desiree R. Espinueva, Delane F. Snyder, Jason S. eNeuro Research Article: New Research Adult neurogenesis modifies hippocampal circuits and behavior, but removing newborn neurons does not consistently alter spatial processing, a core function of the hippocampus. Additionally, little is known about sex differences in neurogenesis since few studies have compared males and females. Since adult-born neurons regulate the stress response, we hypothesized that spatial functions may be more prominent under aversive conditions and may differ between males and females given sex differences in stress responding. We therefore trained intact and neurogenesis-deficient rats in the spatial water maze at temperatures that vary in their degree of aversiveness. In the standard water maze, ablating neurogenesis did not alter spatial learning in either sex. However, in cold water, ablating neurogenesis had divergent sex-dependent effects: relative to intact rats, male neurogenesis-deficient rats were slower to escape the maze and female neurogenesis-deficient rats were faster. Neurogenesis promoted temperature-related changes in search strategy in females, but it promoted search strategy stability in males. Females displayed greater recruitment (Fos expression) of the dorsal hippocampus than males, particularly in cold water. However, blocking neurogenesis did not alter Fos expression in either sex. Finally, morphologic analyses revealed greater experience-dependent plasticity in males. Adult-born neurons in males and females had similar morphology at baseline but training increased spine density and reduced presynaptic terminal size, specifically in males. Collectively, these findings indicate that adult-born neurons contribute to spatial learning in stressful conditions and they provide new evidence for sex differences in their behavioral functions. Society for Neuroscience 2022-05-11 /pmc/articles/PMC9116935/ /pubmed/35473765 http://dx.doi.org/10.1523/ENEURO.0054-22.2022 Text en Copyright © 2022 O’Leary et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
O’Leary, Timothy P.
Askari, Baran
Lee, Bonnie H.
Darby, Kathryn
Knudson, Cypress
Ash, Alyssa M.
Seib, Desiree R.
Espinueva, Delane F.
Snyder, Jason S.
Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats
title Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats
title_full Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats
title_fullStr Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats
title_full_unstemmed Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats
title_short Sex Differences in the Spatial Behavior Functions of Adult-Born Neurons in Rats
title_sort sex differences in the spatial behavior functions of adult-born neurons in rats
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9116935/
https://www.ncbi.nlm.nih.gov/pubmed/35473765
http://dx.doi.org/10.1523/ENEURO.0054-22.2022
work_keys_str_mv AT olearytimothyp sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT askaribaran sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT leebonnieh sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT darbykathryn sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT knudsoncypress sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT ashalyssam sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT seibdesireer sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT espinuevadelanef sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats
AT snyderjasons sexdifferencesinthespatialbehaviorfunctionsofadultbornneuronsinrats