{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T11:19:52Z","timestamp":1780399192191,"version":"3.54.1"},"reference-count":15,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,9,2]],"date-time":"2024-09-02T00:00:00Z","timestamp":1725235200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,9,2]],"date-time":"2024-09-02T00:00:00Z","timestamp":1725235200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["RGPIN-2018-05135"],"award-info":[{"award-number":["RGPIN-2018-05135"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Brain"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Aerobic exercise has many effects on brain function, particularly at the hippocampus. Exercise has been shown to increase the rate of adult neurogenesis within the dentate gyrus and decrease the density of perineuronal nets in area CA1. The relationship between the rate of neurogenesis and the density of perineuronal nets in CA1 is robust; however, these studies only ever examined these effects across longer time scales, with running manipulations of 4 weeks or longer. With such long periods of manipulation, the precise temporal nature of the relationship between running-induced neurogenesis and reduced perineuronal net density in CA1 is unknown. Here, we provided male and female mice with home cage access to running wheels for 0, 1, 2, or 4 weeks and quantified hippocampal neurogenesis and CA1 perineuronal net density. In doing so, we observed a 2-week delay period prior to the increase in neurogenesis, which coincided with the same delay prior to decreased CA1 perineuronal net density. These results highlight the closely linked temporal relationship between running-induced neurogenesis and decreased perineuronal net expression in CA1.<\/jats:p>","DOI":"10.1186\/s13041-024-01138-x","type":"journal-article","created":{"date-parts":[[2024,9,2]],"date-time":"2024-09-02T16:02:36Z","timestamp":1725292956000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Running-induced neurogenesis reduces CA1 perineuronal net density without substantial temporal delay"],"prefix":"10.1186","volume":"17","author":[{"given":"Dylan J.","family":"Terstege","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Duneesha","family":"Goonetilleke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cindy K.","family":"Barha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7968-8973","authenticated-orcid":false,"given":"Jonathan R.","family":"Epp","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,9,2]]},"reference":[{"key":"1138_CR1","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1016\/j.nlm.2006.11.003","volume":"87","author":"B Winter","year":"2007","unstructured":"Winter B, Breitenstein C, Mooren FC, Voelker K, Fobker M, Lechtermann A, et al. High impact running improves learning. Neurobiol Learn Mem. 2007;87:597\u2013609.","journal-title":"Neurobiol Learn Mem"},{"key":"1138_CR2","first-page":"1","volume":"2","author":"SL Aghjayan","year":"2022","unstructured":"Aghjayan SL, Bournias T, Kang C, Zhou X, Stillman CM, Donofry SD, et al. Aerobic exercise improves episodic memory in late adulthood: a systematic review and meta-analysis. Commun Med (Lond). 2022;2:1\u201311.","journal-title":"Commun Med (Lond)"},{"key":"1138_CR3","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1038\/35066584","volume":"410","author":"TJ Shors","year":"2001","unstructured":"Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature. 2001;410:372\u20136.","journal-title":"Nature"},{"key":"1138_CR4","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.neurobiolaging.2017.01.002","volume":"52","author":"B Xu","year":"2017","unstructured":"Xu B, Sun A, He Y, Qian F, Liu L, Chen Y, et al. Running-induced memory enhancement correlates with the preservation of thin spines in the hippocampal area CA1 of old C57BL\/6 mice. Neurobiol Aging. 2017;52:106\u201316.","journal-title":"Neurobiol Aging"},{"key":"1138_CR5","doi-asserted-by":"publisher","first-page":"2749","DOI":"10.1002\/cne.25354","volume":"530","author":"C-X Huang","year":"2022","unstructured":"Huang C-X, Zhang L, Xiao Q, Li C, Qiu X, Chao F-L, et al. Effects of 4-month running exercise on the spatial learning ability and white matter volume and microvessels of middle\u2010aged female and male rats. J Comp Neurol. 2022;530:2749\u201361.","journal-title":"J Comp Neurol"},{"key":"1138_CR6","doi-asserted-by":"publisher","first-page":"598","DOI":"10.1126\/science.1248903","volume":"344","author":"KG Akers","year":"2014","unstructured":"Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, Hsiang H-LL, et al. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science. 2014;344:598\u2013602.","journal-title":"Science"},{"key":"1138_CR7","doi-asserted-by":"publisher","first-page":"10838","DOI":"10.1038\/ncomms10838","volume":"7","author":"JR Epp","year":"2016","unstructured":"Epp JR, Silva Mera R, K\u00f6hler S, Josselyn SA, Frankland PW. Neurogenesis-mediated forgetting minimizes proactive interference. Nat Commun. 2016;7:10838.","journal-title":"Nat Commun"},{"key":"1138_CR8","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1186\/s13041-021-00808-4","volume":"14","author":"GA Scott","year":"2021","unstructured":"Scott GA, Terstege DJ, Roebuck AJ, Gorzo KA, Vu AP, Howland JG, et al. Adult neurogenesis mediates forgetting of multiple types of memory in the rat. Mol Brain. 2021;14:97.","journal-title":"Mol Brain"},{"key":"1138_CR9","doi-asserted-by":"publisher","first-page":"7016","DOI":"10.1038\/s41598-022-10947-w","volume":"12","author":"A Evans","year":"2022","unstructured":"Evans A, Terstege DJ, Scott GA, Tsutsui M, Epp JR. Neurogenesis mediated plasticity is associated with reduced neuronal activity in CA1 during context fear memory retrieval. Sci Rep. 2022;12:7016.","journal-title":"Sci Rep"},{"key":"1138_CR10","doi-asserted-by":"publisher","first-page":"e86237","DOI":"10.1371\/journal.pone.0086237","volume":"9","author":"C-A Gr\u00e9goire","year":"2014","unstructured":"Gr\u00e9goire C-A, Bonenfant D, Le Nguyen A, Aumont A, Fernandes KJL. Untangling the influences of voluntary running, environmental complexity, social housing and stress on adult hippocampal neurogenesis. PLoS ONE. 2014;9:e86237.","journal-title":"PLoS ONE"},{"key":"1138_CR11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.neuroscience.2021.08.022","volume":"475","author":"JR Epp","year":"2021","unstructured":"Epp JR, Botly LCP, Josselyn SA, Frankland PW. Voluntary exercise increases neurogenesis and mediates forgetting of complex paired associates memories. Neuroscience. 2021;475:1\u20139.","journal-title":"Neuroscience"},{"key":"1138_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-020-20241-w","volume":"12","author":"AC Christensen","year":"2021","unstructured":"Christensen AC, Lensj\u00f8 KK, Lepper\u00f8d ME, Dragly S-A, Sutterud H, Blackstad JS, et al. Perineuronal nets stabilize the grid cell network. Nat Commun. 2021;12:1\u201317.","journal-title":"Nat Commun"},{"key":"1138_CR13","doi-asserted-by":"publisher","unstructured":"Shi W, Wei X, Wang X, Du S, Liu W, Song J, S A. Perineuronal nets protect long-term memory by limiting activity-dependent inhibition from parvalbumin interneurons. Proc Natl Acad Sci U. 2019; https:\/\/doi.org\/10.1073\/pnas.1902680116","DOI":"10.1073\/pnas.1902680116"},{"key":"1138_CR14","doi-asserted-by":"publisher","first-page":"862","DOI":"10.1002\/hipo.23503","volume":"33","author":"L Liu","year":"2023","unstructured":"Liu L, Zhang Y, Men S, Li X, Hou S-T, Ju J. Elimination of perineuronal nets in CA1 disrupts GABA release and long-term contextual fear memory retention. Hippocampus. 2023;33:862\u201371.","journal-title":"Hippocampus"},{"key":"1138_CR15","doi-asserted-by":"publisher","first-page":"e00499","DOI":"10.1016\/j.ohx.2023.e00499","volume":"17","author":"DJ Terstege","year":"2024","unstructured":"Terstege DJ, Epp JR. PAW, a cost-effective and open-source alternative to commercial rodent running wheels. HardwareX. 2024;17:e00499.","journal-title":"HardwareX"}],"container-title":["Molecular Brain"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13041-024-01138-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13041-024-01138-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13041-024-01138-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,2]],"date-time":"2024-09-02T16:04:23Z","timestamp":1725293063000},"score":1,"resource":{"primary":{"URL":"https:\/\/molecularbrain.biomedcentral.com\/articles\/10.1186\/s13041-024-01138-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,2]]},"references-count":15,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["1138"],"URL":"https:\/\/doi.org\/10.1186\/s13041-024-01138-x","relation":{},"ISSN":["1756-6606"],"issn-type":[{"value":"1756-6606","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,2]]},"assertion":[{"value":"1 August 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 August 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 September 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Experiments were conducted in accordance with the policies and guidelines of the Canadian Council on Animal Care Guidelines and were approved by the University of Calgary Animal Care Committee.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"64"}}