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Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens

Memory disruption commonly follows chronic stress, whereas acute stressors are generally benign. However, acute traumas such as mass shootings or natural disasters—lasting minutes to hours and consisting of simultaneous physical, social, and emotional stresses—are increasingly recognized as signific...

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Autores principales: Hokenson, Rachael E., Alam, Yasmine H., Short, Annabel K., Jung, Sunhee, Jang, Cholsoon, Baram, Tallie Z.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9492881/
https://www.ncbi.nlm.nih.gov/pubmed/36160685
http://dx.doi.org/10.3389/fnbeh.2022.984494
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author Hokenson, Rachael E.
Alam, Yasmine H.
Short, Annabel K.
Jung, Sunhee
Jang, Cholsoon
Baram, Tallie Z.
author_facet Hokenson, Rachael E.
Alam, Yasmine H.
Short, Annabel K.
Jung, Sunhee
Jang, Cholsoon
Baram, Tallie Z.
author_sort Hokenson, Rachael E.
collection PubMed
description Memory disruption commonly follows chronic stress, whereas acute stressors are generally benign. However, acute traumas such as mass shootings or natural disasters—lasting minutes to hours and consisting of simultaneous physical, social, and emotional stresses—are increasingly recognized as significant risk factors for memory problems and PTSD. Our prior work has revealed that these complex stresses (concurrent multiple acute stresses: MAS) disrupt hippocampus-dependent memory in male rodents. In females, the impacts of MAS are estrous cycle-dependent: MAS impairs memory during early proestrus (high estrogens phase), whereas the memory of female mice stressed during estrus (low estrogens phase) is protected. Female memory impairments limited to high estrogens phases suggest that higher levels of estrogens are necessary for MAS to disrupt memory, supported by evidence that males have higher hippocampal estradiol than estrous females. To test the role of estrogens in stress-induced memory deficits, we blocked estrogen production using aromatase inhibitors. A week of blockade protected male and female mice from MAS-induced memory disturbances, suggesting that high levels of estrogens are required for stress-provoked memory impairments in both males and females. To directly quantify 17β-estradiol in murine hippocampus we employed both ELISA and mass spectrometry and identified significant confounders in both procedures. Taken together, the cross-cycle and aromatase studies in males and females support the role for high hippocampal estrogens in mediating the effect of complex acute stress on memory. Future studies focus on the receptors involved, the longevity of these effects, and their relation to PTSD-like behaviors in experimental models.
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spelling pubmed-94928812022-09-23 Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens Hokenson, Rachael E. Alam, Yasmine H. Short, Annabel K. Jung, Sunhee Jang, Cholsoon Baram, Tallie Z. Front Behav Neurosci Behavioral Neuroscience Memory disruption commonly follows chronic stress, whereas acute stressors are generally benign. However, acute traumas such as mass shootings or natural disasters—lasting minutes to hours and consisting of simultaneous physical, social, and emotional stresses—are increasingly recognized as significant risk factors for memory problems and PTSD. Our prior work has revealed that these complex stresses (concurrent multiple acute stresses: MAS) disrupt hippocampus-dependent memory in male rodents. In females, the impacts of MAS are estrous cycle-dependent: MAS impairs memory during early proestrus (high estrogens phase), whereas the memory of female mice stressed during estrus (low estrogens phase) is protected. Female memory impairments limited to high estrogens phases suggest that higher levels of estrogens are necessary for MAS to disrupt memory, supported by evidence that males have higher hippocampal estradiol than estrous females. To test the role of estrogens in stress-induced memory deficits, we blocked estrogen production using aromatase inhibitors. A week of blockade protected male and female mice from MAS-induced memory disturbances, suggesting that high levels of estrogens are required for stress-provoked memory impairments in both males and females. To directly quantify 17β-estradiol in murine hippocampus we employed both ELISA and mass spectrometry and identified significant confounders in both procedures. Taken together, the cross-cycle and aromatase studies in males and females support the role for high hippocampal estrogens in mediating the effect of complex acute stress on memory. Future studies focus on the receptors involved, the longevity of these effects, and their relation to PTSD-like behaviors in experimental models. Frontiers Media S.A. 2022-09-08 /pmc/articles/PMC9492881/ /pubmed/36160685 http://dx.doi.org/10.3389/fnbeh.2022.984494 Text en Copyright © 2022 Hokenson, Alam, Short, Jung, Jang and Baram. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Behavioral Neuroscience
Hokenson, Rachael E.
Alam, Yasmine H.
Short, Annabel K.
Jung, Sunhee
Jang, Cholsoon
Baram, Tallie Z.
Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
title Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
title_full Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
title_fullStr Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
title_full_unstemmed Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
title_short Sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
title_sort sex-dependent effects of multiple acute concurrent stresses on memory: a role for hippocampal estrogens
topic Behavioral Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9492881/
https://www.ncbi.nlm.nih.gov/pubmed/36160685
http://dx.doi.org/10.3389/fnbeh.2022.984494
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