{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,5]],"date-time":"2026-09-05T18:08:35Z","timestamp":1788631715888,"version":"build-2803163510"},"reference-count":48,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2017,9,20]],"date-time":"2017-09-20T00:00:00Z","timestamp":1505865600000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Brain Struct Funct"],"published-print":{"date-parts":[[2018,3]]},"DOI":"10.1007\/s00429-017-1521-0","type":"journal-article","created":{"date-parts":[[2017,9,20]],"date-time":"2017-09-20T11:24:53Z","timestamp":1505906693000},"page":"749-767","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Voluntary running-enhanced synaptic plasticity, learning and memory are mediated by Notch1 signal pathway in C57BL mice"],"prefix":"10.1007","volume":"223","author":[{"given":"Xiaochen","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunxiao","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongqiang","family":"Yin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5212-0053","authenticated-orcid":false,"given":"Zhuo","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,9,20]]},"reference":[{"key":"1521_CR1","doi-asserted-by":"crossref","first-page":"10484","DOI":"10.1523\/JNEUROSCI.4721-09.2010","volume":"30","author":"JL Ables","year":"2010","unstructured":"Ables JL et al (2010) Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci 30:10484\u201310492","journal-title":"J Neurosci"},{"key":"1521_CR2","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/j.neuron.2011.01.004","volume":"69","author":"L Alberi","year":"2011","unstructured":"Alberi L et al (2011) Activity-induced notch signaling in neurons requires Arc\/Arg3.1 and is essential for synaptic plasticity in hippocampal networks. Neuron 69:437\u2013444","journal-title":"Neuron"},{"key":"1521_CR3","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1038\/nature04940","volume":"442","author":"AT Andreas","year":"2006","unstructured":"Andreas AT et al (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823\u2013826","journal-title":"Nature"},{"key":"1521_CR4","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1124\/mol.51.4.535","volume":"51","author":"C Behl","year":"1997","unstructured":"Behl C, Skutella T, Lezoualc\u2019H F, Post A, Widmann M, Newton CJ, Holsboer F (1997) Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535\u2013541","journal-title":"Mol Pharmacol"},{"key":"1521_CR5","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.1038\/nprot.2006.205","volume":"1","author":"RA Bevins","year":"2006","unstructured":"Bevins RA, Joyce B (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study \u2018recognition memory\u2019. Nat Protoc 1:1306\u20131311","journal-title":"Nat Protoc"},{"key":"1521_CR6","first-page":"575","volume":"13","author":"TV Bliss","year":"1993","unstructured":"Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Mol Cancer Res 13:575\u2013583","journal-title":"Mol Cancer Res"},{"key":"1521_CR7","doi-asserted-by":"crossref","first-page":"447","DOI":"10.3389\/fncel.2015.00447","volume":"9","author":"E Brai","year":"2015","unstructured":"Brai E et al (2015) Notch1 regulates hippocampal plasticity through interaction with the Reelin pathway, glutamatergic transmission and CREB signaling. Front Cell Neurosci 9:447","journal-title":"Front Cell Neurosci"},{"key":"1521_CR8","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1111\/j.1460-9568.2010.07410.x","volume":"32","author":"MD Brandt","year":"2010","unstructured":"Brandt MD, Maass A, Kempermann G, Storch A (2010) Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. Eur J Neurosci 32:1256\u20131264","journal-title":"Eur J Neurosci"},{"key":"1521_CR9","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1093\/gerona\/62.1.9","volume":"62","author":"KA Carey","year":"2007","unstructured":"Carey KA, Farnfield MM, Tarquinio SD, Cameron-Smith D (2007) Impaired expression of Notch signaling genes in aged human skeletal muscle. J Gerontol 62:9\u201317","journal-title":"J Gerontol"},{"key":"1521_CR10","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.neuron.2006.08.033","volume":"52","author":"S Chowdhury","year":"2006","unstructured":"Chowdhury S et al (2006) Arc\/Arg3. 1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52:445\u2013459","journal-title":"Neuron"},{"key":"1521_CR11","doi-asserted-by":"crossref","first-page":"1348","DOI":"10.1016\/S0960-9822(03)00492-5","volume":"13","author":"M Costa","year":"2003","unstructured":"Costa M, Honjo T, Silva AJ (2003) Learning and memory deficits in notch mutant mice. Curr Biol 13:1348\u20131354","journal-title":"Curr Biol"},{"key":"1521_CR12","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1038\/19083","volume":"398","author":"B De Strooper","year":"1999","unstructured":"De Strooper B et al (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398:518\u2013522","journal-title":"Nature"},{"key":"1521_CR13","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1038\/3305","volume":"4","author":"PS Eriksson","year":"1998","unstructured":"Eriksson PS, Perfilieva E, Bj\u00f6rkeriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313\u20131317","journal-title":"Nat Med"},{"key":"1521_CR14","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.nlm.2005.08.004","volume":"84","author":"AE Fitchett","year":"2005","unstructured":"Fitchett AE, Collins SA, Barnard CJ, Cassaday HJ (2005) Subordinate male mice show long-lasting differences in spatial learning that persist when housed alone. Neurobiol Learn Mem 84:247\u2013251","journal-title":"Neurobiol Learn Mem"},{"key":"1521_CR15","volume-title":"The mouse brain: in stereotaxic coordinates","author":"KBJ Franklin","year":"2001","unstructured":"Franklin KBJ, Paxinos G (2001) The mouse brain: in stereotaxic coordinates. Academic Press, San Diego"},{"key":"1521_CR16","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1007\/s12035-016-9687-7","volume":"54","author":"J Fu","year":"2016","unstructured":"Fu J, Hui W, Jing G, Mei Y, Wang R, Zhuo Y, Tao Z (2016) Rapamycin effectively impedes melamine-induced impairments of cognition and synaptic plasticity in Wistar rats. Mol Neurobiol 54:819\u2013832","journal-title":"Mol Neurobiol"},{"key":"1521_CR17","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1002\/hipo.20634","volume":"20","author":"J Fuss","year":"2010","unstructured":"Fuss J et al (2010) Voluntary exercise induces anxiety-like behavior in adult C57BL\/6J mice correlating with hippocampal neurogenesis. Hippocampus 20:364\u2013376","journal-title":"Hippocampus"},{"key":"1521_CR18","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.tox.2015.08.011","volume":"337","author":"J Gao","year":"2015","unstructured":"Gao J, Zhang X, Yu M, Ren G, Yang Z (2015) Cognitive deficits induced by multi-walled carbon nanotubes via the autophagic pathway. Toxicology 337:21\u201329","journal-title":"Toxicology"},{"key":"1521_CR19","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0301-0082(00)00025-3","volume":"63","author":"LM Garcia-Segura","year":"2001","unstructured":"Garcia-Segura LM, Azcoitia I, Doncarlos LL (2001) Neuroprotection by estradiol. Prog Neurobiol 63:29","journal-title":"Prog Neurobiol"},{"key":"1521_CR20","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1002\/cne.1059","volume":"436","author":"DK Irvin","year":"2001","unstructured":"Irvin DK, Zurcher SD, Nguyen T, Weinmaster G, Kornblum HI (2001) Expression patterns of Notch1, Notch2, and Notch3 suggest multiple functional roles for the Notch-DSL signaling system during brain development. J Comp Neurol 436:167\u2013181","journal-title":"J Comp Neurol"},{"key":"1521_CR21","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1113\/jphysiol.2002.031369","volume":"546","author":"BQ Jean-Claude","year":"2003","unstructured":"Jean-Claude BQ, Rodrigo A (2003) PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J Physiol 546:859\u2013867","journal-title":"J Physiol"},{"key":"1521_CR22","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.brainres.2003.09.060","volume":"995","author":"M-L Jiang","year":"2004","unstructured":"Jiang M-L, Han T-Z, Pang W, Li L (2004) Gender-and age-specific impairment of rat performance in the Morris water maze following prenatal exposure to an MRI magnetic field. Brain Res 995:140\u2013144","journal-title":"Brain Res"},{"key":"1521_CR23","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.bbamcr.2008.10.002","volume":"1793","author":"YH Jin","year":"2009","unstructured":"Jin YH et al (2009) Beta-catenin modulates the level and transcriptional activity of Notch1\/NICD through its direct interaction. Biochem Biophys Acta 1793:290\u2013299","journal-title":"Biochem Biophys Acta"},{"key":"1521_CR24","doi-asserted-by":"crossref","first-page":"245","DOI":"10.5483\/BMBRep.2009.42.5.245","volume":"42","author":"M Johnson","year":"2009","unstructured":"Johnson M, Ables J, Eisch A (2009) Cell-intrinsic signals that regulate adult neurogenesis in vivo: insights from inducible approaches. BMB Rep 42:245\u2013259","journal-title":"BMB Rep"},{"key":"1521_CR25","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1097\/WNR.0000000000000419","volume":"26","author":"J Li","year":"2015","unstructured":"Li J, Wen PY, Li WW, Zhou J (2015) Upregulation effects of Tanshinone IIA on the expressions of NeuN, Nissl body, and I\u03baB and downregulation effects on the expressions of GFAP and NF-\u03baB in the brain tissues of rat models of Alzheimer\u2019s disease. Neuroreport 26:758\u2013766","journal-title":"Neuroreport"},{"key":"1521_CR26","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.bbr.2016.03.023","volume":"305","author":"Z Li","year":"2016","unstructured":"Li Z, Hao S, Yin H, Gao J, Yang Z (2016) Autophagy ameliorates cognitive impairment through activation of PVT1 and apoptosis in diabetes mice. Behav Brain Res 305:265\u2013277","journal-title":"Behav Brain Res"},{"key":"1521_CR27","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/0092-8674(95)90294-5","volume":"80","author":"CE Lindsell","year":"1995","unstructured":"Lindsell CE, Shawber CJ, Boulter J, Weinmaster G (1995) Jagged: a mammalian ligand that activates Notch1. Cell 80:909\u2013917","journal-title":"Cell"},{"key":"1521_CR28","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1126\/science.285.5435.1870","volume":"285","author":"RC Malenka","year":"1999","unstructured":"Malenka RC, Nicoll RA (1999) Long-term potentiation\u2013a decade of progress? Science 285:1870\u20131874","journal-title":"Science"},{"key":"1521_CR29","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1177\/0269881108093842","volume":"24","author":"S Mclean","year":"2010","unstructured":"Mclean S, Grayson B, Harris M, Protheroe C, Woolley M, Neill J (2010) Isolation rearing impairs novel object recognition and attentional set shifting performance in female rats. J Psychopharmacol 24:57\u201363","journal-title":"J Psychopharmacol"},{"key":"1521_CR30","first-page":"1","volume":"65","author":"Y Mei","year":"2015","unstructured":"Mei Y, Yuan Z, Chen X, Tao Z (2015) Antidepressant-like effects and possible mechanisms of amantadine on cognitive and synaptic deficits in a rat model of chronic stress. Stress 65:1\u201332","journal-title":"Stress"},{"key":"1521_CR31","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1007\/s12264-013-1375-2","volume":"30","author":"Z Nan","year":"2014","unstructured":"Nan Z, Xing M, Wang Y, Hao L, Zhuo Y, Shi F, Yan C (2014) Hydroxysafflor yellow A improves learning and memory in a rat model of vascular dementia by increasing VEGF and NR1 in the hippocampus. Neurosci Bull 30:417\u2013424","journal-title":"Neurosci Bull"},{"key":"1521_CR32","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.bbr.2013.02.009","volume":"245","author":"T Nishijima","year":"2013","unstructured":"Nishijima T, Tejeda GS, Inoue K, Yamamura Y, Soya H, Trejo JL, Torres-Alem\u00e1n I (2013) Cessation of voluntary wheel running increases anxiety-like behavior and impairs adult hippocampal neurogenesis in mice. Behav Brain Res 245:34\u201341","journal-title":"Behav Brain Res"},{"key":"1521_CR33","first-page":"276","volume":"41","author":"R Niu","year":"2008","unstructured":"Niu R, Sun Z, Wang J, Cheng Z, Wang J (2008) Effects of fluoride and lead on locomotor behavior and expression of nissl body in brain of adult rats. Fluoride 41:276\u2013282","journal-title":"Fluoride"},{"key":"1521_CR34","first-page":"1","volume":"8","author":"A Pan-Vazquez","year":"2015","unstructured":"Pan-Vazquez A et al (2015) Impact of voluntary exercise and housing conditions on hippocampal glucocorticoid receptor, miR-124 and anxiety Molecular. Brain 8:1\u201312","journal-title":"Brain"},{"key":"1521_CR35","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1083\/jcb.53.1.24","volume":"53","author":"DL Price","year":"1972","unstructured":"Price DL, Porter KR (1972) The response of ventral horn neurons to axonal transection. J Cell Biol 53:24\u201337","journal-title":"J Cell Biol"},{"key":"1521_CR36","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1093\/cercor\/bhs086","volume":"23","author":"Y Qi","year":"2013","unstructured":"Qi Y, Hu N-W, Rowan MJ (2013) Switching off LTP: mGlu and NMDA receptor-dependent novelty exploration-induced depotentiation in the rat hippocampus. Cereb Cortex 23:932\u2013939","journal-title":"Cereb Cortex"},{"key":"1521_CR37","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1126\/science.284.5421.1845","volume":"284","author":"R Sattler","year":"1999","unstructured":"Sattler R, Xiong Z, Lu WY, Hafner M, Macdonald JF, Tymianski M (1999) Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284:1845\u20131848","journal-title":"Science"},{"key":"1521_CR38","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1038\/30756","volume":"393","author":"EH Schroeter","year":"1998","unstructured":"Schroeter EH, Kisslinger JA, Kopan R (1998) Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393:382\u2013386","journal-title":"Nature"},{"key":"1521_CR39","doi-asserted-by":"crossref","first-page":"3643","DOI":"10.1111\/j.1460-9568.2012.08279.x","volume":"36","author":"M Sibbe","year":"2012","unstructured":"Sibbe M, H\u00e4ussler U, Dieni S, Althof D, Haas CA, Frotscher M (2012) Experimental epilepsy affects Notch1 signalling and the stem cell pool in the dentate gyrus. Eur J Neurosci 36:3643","journal-title":"Eur J Neurosci"},{"key":"1521_CR40","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1038\/nn1668","volume":"9","author":"AM Stranahan","year":"2006","unstructured":"Stranahan AM, Khalil D, Gould E (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9:526\u2013533","journal-title":"Nat Neurosci"},{"key":"1521_CR41","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1038\/nn1668","volume":"9","author":"K Sugioka","year":"2006","unstructured":"Sugioka K, Setsu T, Terashima T (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9:526\u2013533","journal-title":"Nat Neurosci"},{"key":"1521_CR42","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1002\/jcp.10208","volume":"194","author":"I Tatsuya","year":"2003","unstructured":"Tatsuya I, Larry K, Yasuo H (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194:237\u2013255","journal-title":"J Cell Physiol"},{"key":"1521_CR43","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1002\/bies.20012","volume":"26","author":"F Valtorta","year":"2004","unstructured":"Valtorta F, Pennuto MD, Benfenati F (2004) Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? Bioessays News Rev Mol Cell Dev Biol 26:445\u2013453","journal-title":"Bioessays News Rev Mol Cell Dev Biol"},{"key":"1521_CR44","doi-asserted-by":"crossref","first-page":"13427","DOI":"10.1073\/pnas.96.23.13427","volume":"96","author":"H Praag Van","year":"1999","unstructured":"Van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci 96:13427\u201313431","journal-title":"Proc Natl Acad Sci"},{"key":"1521_CR45","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1111\/j.1601-183X.2004.00106.x","volume":"4","author":"V V\u00f5ikar","year":"2005","unstructured":"V\u00f5ikar V, Polus A, Vasar E, Rauvala H (2005) Long-term individual housing in C57BL\/6J and DBA\/2 mice: assessment of behavioral consequences. Genes Brain Behav 4:240\u2013252","journal-title":"Genes Brain Behav"},{"key":"1521_CR46","doi-asserted-by":"crossref","first-page":"9458","DOI":"10.1073\/pnas.0308126101","volume":"101","author":"Y Wang","year":"2004","unstructured":"Wang Y et al (2004) Involvement of Notch signaling in hippocampal synaptic plasticity. Proc Natl Acad Sci USA 101:9458\u20139462","journal-title":"Proc Natl Acad Sci USA"},{"key":"1521_CR47","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1002\/hipo.22544","volume":"26","author":"J Yang","year":"2015","unstructured":"Yang J, Yang C, Liu C, Tao Z, Zhuo Y (2015) Paradoxical effects of VEGF on synaptic activity partially involved in notch1 signaling in the mouse hippocampus. Hippocampus 26:589\u2013600","journal-title":"Hippocampus"},{"key":"1521_CR48","doi-asserted-by":"crossref","first-page":"15810","DOI":"10.1073\/pnas.1415219111","volume":"111","author":"SY Yau","year":"2014","unstructured":"Yau SY et al (2014) Physical exercise-induced hippocampal neurogenesis and antidepressant effects are mediated by the adipocyte hormone adiponectin. Proc Natl Acad Sci 111:15810\u201315815","journal-title":"Proc Natl Acad Sci"}],"container-title":["Brain Structure and Function"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00429-017-1521-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00429-017-1521-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00429-017-1521-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,27]],"date-time":"2024-06-27T03:16:00Z","timestamp":1719458160000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00429-017-1521-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,9,20]]},"references-count":48,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2018,3]]}},"alternative-id":["1521"],"URL":"https:\/\/doi.org\/10.1007\/s00429-017-1521-0","relation":{},"ISSN":["1863-2653","1863-2661"],"issn-type":[{"value":"1863-2653","type":"print"},{"value":"1863-2661","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,9,20]]}}}