{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T13:59:31Z","timestamp":1787320771633,"version":"build-2736575974"},"reference-count":76,"publisher":"National Academy of Sciences","issue":"52","license":[{"start":{"date-parts":[[2020,6,23]],"date-time":"2020-06-23T00:00:00Z","timestamp":1592870400000},"content-version":"vor","delay-in-days":183,"URL":"https:\/\/www.pnas.org\/site\/aboutpnas\/licenses.xhtml"}],"funder":[{"DOI":"10.13039\/100000025","name":"HHS | NIH | National Institute of Mental Health","doi-asserted-by":"publisher","award":["MH-58846"],"award-info":[{"award-number":["MH-58846"]}],"id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["HD-090925"],"award-info":[{"award-number":["HD-090925"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000097","name":"HHS | NIH | National Center for Research Resources","doi-asserted-by":"publisher","award":["P51RR165"],"award-info":[{"award-number":["P51RR165"]}],"id":[{"id":"10.13039\/100000097","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2019,12,26]]},"abstract":"<jats:p>Nonhuman primates provide highly valuable animal models that have significantly advanced our understanding of numerous behavioral and biological phenomena in humans. Here, we reviewed a series of developmental neuropsychological studies that informed us on the timing of development of the hippocampus and of hippocampal-dependent cognitive functions in primates. Data indicate that, in primates, the emergence of adult-like proficiency on behavioral tasks sensitive to hippocampal dysfunction is a stepwise process and reflects the gradual maturation of different hippocampal circuits and their connections with other neural structures. Profound and persistent memory loss resulting from insult to the hippocampus in infancy was absent in early infancy but became evident later in childhood and persisted in adulthood, indicating very little sparing or recovery of function. Finally, the early hippocampal insult resulted in both adaptive and maladaptive neuroplasticity: i.e., sparing contextual memory, but affecting working memory processes as well as emotional reactivity and hypothalamic\u2013pituitary\u2013adrenal (HPA) axis functioning. The results provide significant information on the emergence of hippocampal-dependent functions in humans, on the time course of memory impairment in human cases with early hippocampal insult, and on the clinical implication of the hippocampus in developmental neuropsychiatric disorders.<\/jats:p>","DOI":"10.1073\/pnas.1902278116","type":"journal-article","created":{"date-parts":[[2019,12,23]],"date-time":"2019-12-23T20:35:36Z","timestamp":1577133336000},"page":"26210-26216","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":20,"title":["Nonhuman primate models of hippocampal development and dysfunction"],"prefix":"10.1073","volume":"116","author":[{"given":"Jocelyne","family":"Bachevalier","sequence":"first","affiliation":[{"name":"Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329;"},{"name":"Department of Psychology, Emory University, Atlanta, GA 30329"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2019,12,23]]},"reference":[{"key":"e_1_3_3_1_2","doi-asserted-by":"publisher","DOI":"10.1093\/acprof:oso\/9780199592388.003.0003"},{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1093\/acprof:oso\/9780199592388.003.0005"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1093\/acprof:oso\/9780199592388.001.0001"},{"key":"e_1_3_3_4_2","first-page":"17","volume-title":"The Hippocampus: New Vista","author":"Nadel L.","year":"1989","unstructured":"L. Nadel, J. Willner, \u201cSome implications of postnatal maturation of the hippocampus\u201d in The Hippocampus: New Vista, V. Chan-Palay, C. Kohler, Eds. (Alan R. Liss, New York, 1989), pp. 17\u201331."},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1188210"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1002\/wcs.1424"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2014.04.009"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbr.2008.11.039"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.neuro.31.061307.090723"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.20-15-05827.2000"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-662-03628-0"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.20688"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.22271"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.450050308"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1002\/cne.903550111"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1093\/acprof:oso\/9780199592388.003.0002"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1159\/000096222"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1038\/tp.2012.105"},{"key":"e_1_3_3_19_2","first-page":"187","volume-title":"Handbook of Developmental Cognitive Neuroscience","author":"Seress L.","year":"2009","unstructured":"L. Seress, H. Abraham, \u201cPre- and post-natal morphological development of the human hippocampal formation\u201d in Handbook of Developmental Cognitive Neuroscience, C. A. Nelson, M. Luciana, Eds. (MIT Press, Cambridge, MA, ed. 2, 2009), pp. 187\u2013212.","edition":"2"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.08-12-04693.1988"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1101\/lm.35100"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.dcn.2014.07.002"},{"key":"e_1_3_3_23_2","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/B978-0-12-812012-5.00011-2","volume-title":"Handbook of Object Novelty Recognition","author":"Bachevalier J.","year":"2018","unstructured":"J. Bachevalier, \u201cDevelopmental trajectories of object and spatial recognition memory in infant rhesus macaques\u201d in Handbook of Object Novelty Recognition, A. Ennaceur, M. A. De Souza Silva, Eds. (Academic Press, London, 2018), pp. 173\u2013183."},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3763-03.2004"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.20369"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.0022-10.2010"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1139\/y95-191"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.22139"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1017\/S1355617713000799"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1037\/a0031498"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbr.2013.02.007"},{"key":"e_1_3_3_32_2","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1093\/acprof:oso\/9780195340792.003.0006","volume-title":"Origins and Development of Recollection: Perspectives from Psychology and Neuroscience","author":"Ghetti S.","year":"2012","unstructured":"S. Ghetti, K. Lyons, D. DeMaster, \u201cThe development of episodic memory: Binding processes, control processes and introspection on memory states\u201d in Origins and Development of Recollection: Perspectives from Psychology and Neuroscience, S. Ghetti, P. Bauer, Eds. (Oxford University Press, Oxford, 2012), pp. 144\u2013167."},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-1063(1998)8:4<323::AID-HIPO2>3.0.CO;2-I"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(01)00358-X"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbr.2014.07.010"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1037\/bne0000277"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1038\/80655"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1101\/lm.57803"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.conb.2006.10.012"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1093\/cercor\/bhm245"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.5751-11.2012"},{"key":"e_1_3_3_42_2","doi-asserted-by":"publisher","DOI":"10.1162\/jocn_a_01218"},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.nlm.2017.05.012"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.1037\/a0025541"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1991.0158"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.1093\/schbul\/sbr029"},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.1093\/cercor\/bhv019"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/0306-4522(84)90166-0"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1002\/cne.20796"},{"key":"e_1_3_3_50_2","doi-asserted-by":"publisher","DOI":"10.1002\/cne.23498"},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2014.08.059"},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.nlm.2016.04.003"},{"key":"e_1_3_3_53_2","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1002\/hipo.20737","article-title":"Alterations of white matter tracts following neurotoxic hippocampal lesions in macaque monkeys: A diffusion tensor imaging study","volume":"20","author":"Shamy J. L.","year":"2010","unstructured":"J. L. Shamy ., Alterations of white matter tracts following neurotoxic hippocampal lesions in macaque monkeys: A diffusion tensor imaging study. Hippocampus 20, 906\u2013910 (2010).","journal-title":"Hippocampus"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.psyneuen.2016.11.018"},{"key":"e_1_3_3_55_2","doi-asserted-by":"publisher","DOI":"10.1037\/a0012600"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.1002\/dev.20451"},{"key":"e_1_3_3_57_2","doi-asserted-by":"publisher","DOI":"10.1037\/0278-7393.24.1.249"},{"key":"e_1_3_3_58_2","first-page":"113","volume-title":"Memory and Cognitive Processes,","author":"Newcombe N. S.","year":"2004","unstructured":"N. S. Newcombe, \u201cSpatial cognition\u201d in Memory and Cognitive Processes,D. Medin, Ed. (Stevens\u2019 Handbook of Experimental Psychology, John Wiley, New York, ed. 3, 2004), vol. 2, pp. 113\u2013163.","edition":"3"},{"key":"e_1_3_3_59_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.2044-8295.1998.tb02697.x"},{"key":"e_1_3_3_60_2","doi-asserted-by":"publisher","DOI":"10.1037\/0735-7044.110.6.1205"},{"key":"e_1_3_3_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cogpsych.2012.08.001"},{"key":"e_1_3_3_62_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.20193"},{"key":"e_1_3_3_63_2","doi-asserted-by":"publisher","DOI":"10.1093\/cercor\/bht160"},{"key":"e_1_3_3_64_2","doi-asserted-by":"publisher","DOI":"10.1002\/hbm.22576"},{"key":"e_1_3_3_65_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2014.03.019"},{"key":"e_1_3_3_66_2","doi-asserted-by":"publisher","DOI":"10.1101\/lm.021311.110"},{"key":"e_1_3_3_67_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1248903"},{"key":"e_1_3_3_68_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tins.2006.05.008"},{"key":"e_1_3_3_69_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.20836"},{"key":"e_1_3_3_70_2","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.1087"},{"key":"e_1_3_3_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.dcn.2016.06.001"},{"key":"e_1_3_3_72_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2009.09.004"},{"key":"e_1_3_3_73_2","doi-asserted-by":"publisher","DOI":"10.1007\/7854_2010_43"},{"key":"e_1_3_3_74_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-3223(01)01252-5"},{"key":"e_1_3_3_75_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0033291710001170"},{"key":"e_1_3_3_76_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.schres.2009.08.013"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.pnas.org\/syndication\/doi\/10.1073\/pnas.1902278116","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1902278116","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,28]],"date-time":"2024-07-28T23:08:12Z","timestamp":1722208092000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1902278116"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,23]]},"references-count":76,"journal-issue":{"issue":"52","published-print":{"date-parts":[[2019,12,26]]}},"alternative-id":["10.1073\/pnas.1902278116"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1902278116","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,23]]},"assertion":[{"value":"2019-12-23","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}