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      Sex Differences in Maturation and Attrition of Adult Neurogenesis in the Hippocampus

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          Abstract

          Sex differences exist in the regulation of adult neurogenesis in the hippocampus in response to hormones and cognitive training. Here, we investigated the trajectory and maturation rate of adult-born neurons in the dentate gyrus (DG) of male and female rats. Sprague Dawley rats were perfused 2 h, 24 h, one week (1w), 2w, or 3w after bromodeoxyuridine (BrdU) injection, a DNA synthesis marker that labels dividing progenitor cells and their progeny. Adult-born neurons (BrdU/NeuN-ir) matured faster in males compared with females. Males had a greater density of neural stem cells (Sox2-ir) in the dorsal, but not in the ventral, DG and had higher levels of cell proliferation (Ki67-ir) than non-proestrous females. However, males showed a greater reduction in neurogenesis between 1week and 2weeks after mitosis, whereas females showed similar levels of neurogenesis throughout the weeks. The faster maturation and greater attrition of new neurons in males compared with females suggests greater potential for neurogenesis to respond to external stimuli in males and emphasizes the importance of studying sex on adult hippocampal neurogenesis.

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          Adult hippocampal neurogenesis buffers stress responses and depressive behavior

          Jason Snyder, Amélie Soumier, Michelle Brewer … (2011)
          Summary Glucocorticoids are released in response to stressful experiences and serve many beneficial homeostatic functions. However, dysregulation of glucocorticoids is associated with cognitive impairments and depressive illness 1, 2 . In the hippocampus, a brain region densely populated with receptors for stress hormones, stress and glucocorticoids strongly inhibit adult neurogenesis 3 . Decreased neurogenesis has been implicated in the pathogenesis of anxiety and depression, but direct evidence for this role is lacking 4, 5 . Here we show that adult-born hippocampal neurons are required for normal expression of the endocrine and behavioral components of the stress response. Using transgenic and radiation methods to specifically inhibit adult neurogenesis, we find that glucocorticoid levels are slower to recover after moderate stress and are less suppressed by dexamethasone in neurogenesis-deficient mice compared with intact mice, consistent with a role for the hippocampus in regulation of the hypothalamic-pituitary-adrenal (HPA) axis 6, 7 . Relative to controls, neurogenesis-deficient mice showed increased food avoidance in a novel environment after acute stress, increased behavioral despair in the forced swim test, and decreased sucrose preference, a measure of anhedonia. These findings identify a small subset of neurons within the dentate gyrus that are critical for hippocampal negative control of the HPA axis and support a direct role for adult neurogenesis in depressive illness.
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            Reduced fear expression after lesions of the ventral hippocampus.

            Kirsten G Kjelstrup, Frode A Tuvnes, Hill-Aina Steffenach … (2002)
            The hippocampus has a critical role in several fundamental memory operations, including the conditioning of fear to contextual information. We show that the hippocampus is necessary also for unconditioned fear, and that the involved circuitry is at the ventral pole of the hippocampus. Rats with selective hippocampal lesions failed to avoid open arms in an elevated plus-maze and had decreased neuroendocrine stress responses during confinement to a brightly lit chamber. These effects were reproduced by lesions of the ventral half of the hippocampus, but not by damage to the dorsal three-quarters of the hippocampus or the amygdala. Ventral lesions failed to impair contextual fear conditioning or spatial navigation, suggesting that the ventral hippocampus may specifically influence some types of defensive fear-related behavior.
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              A role for adult neurogenesis in spatial long-term memory.

              J.S. Snyder, N.S. Hong, R.J. McDonald … (2005)
              Adult hippocampal neurogenesis has been linked to learning but details of the relationship between neuronal production and memory formation remain unknown. Using low dose irradiation to inhibit adult hippocampal neurogenesis we show that new neurons aged 4-28 days old at the time of training are required for long-term memory in a spatial version of the water maze. This effect of irradiation was specific since long-term memory for a visibly cued platform remained intact. Furthermore, irradiation just before or after water maze training had no effect on learning or long-term memory. Relationships between learning and new neuron survival, as well as proliferation, were investigated but found non-significant. These results suggest a new role for adult neurogenesis in the formation and/or consolidation of long-term, hippocampus-dependent, spatial memories.
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                Author and article information

                Journal
                Journal ID (nlm-ta): eNeuro
                Journal ID (iso-abbrev): eNeuro
                Journal ID (hwp): eneuro
                Journal ID (pmc): eneuro
                Journal ID (publisher-id): eNeuro
                Title: eNeuro
                Publisher: Society for Neuroscience
                ISSN (Electronic): 2373-2822
                Publication date (Electronic preprint): 25 June 2020
                Publication date (Electronic): 17 July 2020
                Publication date Collection: Jul-Aug 2020
                Volume: 7
                Issue: 4
                Electronic Location Identifier: ENEURO.0468-19.2020
                Affiliations
                [1 ]Graduate Program in Neuroscience, University of British Columbia , Vancouver, British Columbia V6T 1Z3, Canada
                [2 ]Department of Psychology, University of British Columbia , Vancouver, British Columbia V6T 1Z3, Canada
                [3 ]Department of Physics and Astronomy, University of British Columbia , Vancouver, British Columbia V6T 1Z3, Canada
                [4 ]Djavad Mowafaghian Centre for Brain Health, University of British Columbia , Vancouver, British Columbia V6T 1Z3, Canada
                Author notes

                The authors declare no competing financial interests.

                Author contributions: S.Y. and L.A.M.G. designed research; S.Y., J.E.J.S., D.T., S.W., and Y.W. performed research; S.Y., J.E.J.S., Y.W., and L.A.M.G. analyzed data; S.Y. and L.A.M.G. wrote the paper.

                This work was supported by the Natural Sciences and Engineering Research Council (NSERC) Discovery Grant RGPIN-2018–04301 (to L.A.M.G.) and by a Izaak Walton Killam Memorial Pre-Doctoral Fellowship (S.Y.).

                Correspondence should be addressed to Liisa A. M. Galea at liisa.galea@ 123456ubc.ca .
                Author information
                https://orcid.org/0000-0003-2874-9972
                Article
                Publisher ID: eN-NWR-0468-19
                DOI: 10.1523/ENEURO.0468-19.2020
                PMC ID: 7369314
                PubMed ID: 32586842
                SO-VID: 0ce5a081-435f-4201-b5d4-976daa625a5e
                Copyright © Copyright © 2020 Yagi et al.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                Date received : 11 November 2019
                Date revision received : 15 June 2020
                Date accepted : 18 June 2020
                Page count
                Figures: 7, Tables: 2, Equations: 0, References: 71, Pages: 14, Words: 00
                Funding
                Funded by: http://doi.org/10.13039/501100000038Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC)
                Award ID: RGPIN-2018-04301
                Funded by: http://doi.org/10.13039/501100004073Killam Trusts (Killam)
                Categories
                Subject: 1
                Subject: Research Article: New Research
                Subject: Cognition and Behavior
                Custom metadata
                cover-date July/August 2020

                Keywords: brdu,dentate gyrus,doublecortin,ki67,cell proliferation,cell survival,sox2
                Data availability:
                Keywords: brdu, dentate gyrus, doublecortin, ki67, cell proliferation, cell survival, sox2

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