{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,3]],"date-time":"2025-11-03T13:42:05Z","timestamp":1762177325877,"version":"3.44.0"},"reference-count":127,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2020,10,1]],"date-time":"2020-10-01T00:00:00Z","timestamp":1601510400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2020,10,1]],"date-time":"2020-10-01T00:00:00Z","timestamp":1601510400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"funder":[{"DOI":"10.13039\/100009790","name":"University at Albany","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009790","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Physiology &amp; Behavior"],"published-print":{"date-parts":[[2020,10]]},"DOI":"10.1016\/j.physbeh.2020.113106","type":"journal-article","created":{"date-parts":[[2020,7,25]],"date-time":"2020-07-25T02:30:57Z","timestamp":1595644257000},"page":"113106","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":3,"special_numbering":"C","title":["Rotated nursing environment with underfeeding: A form of early-life adversity with sex- and age-dependent effects on coping behavior and hippocampal neurogenesis"],"prefix":"10.1016","volume":"225","author":[{"given":"Rose M.","family":"De Guzman","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joanna","family":"Medina","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Angela I.","family":"Saulsbery","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joanna L.","family":"Workman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.physbeh.2020.113106_bib0001","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1016\/S0006-3223(01)01157-X","article-title":"The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies","volume":"49","author":"Heim","year":"2001","journal-title":"Biol. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0002","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1080\/10253890.2017.1343296","article-title":"Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential","volume":"20","author":"Walker","year":"2017","journal-title":"Stress"},{"key":"10.1016\/j.physbeh.2020.113106_bib0003","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1126\/science.1083968","article-title":"Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene","volume":"301","author":"Caspi","year":"2003","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2020.113106_bib0004","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1017\/S0954579411000186","article-title":"Foundations of posttraumatic stress disorder: does early life trauma lead to adult posttraumatic stress disorder?","volume":"23","author":"Pratchett","year":"2011","journal-title":"Dev. Psychopathol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0005","doi-asserted-by":"crossref","first-page":"15","DOI":"10.3109\/10673229.2011.549773","article-title":"Psychiatric outcomes in young children with a history of institutionalization","volume":"19","author":"Bos","year":"2011","journal-title":"Harv. Rev. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0006","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1176\/appi.ajp.2009.08091438","article-title":"Institutional rearing and psychiatric disorders in Romanian preschool children","volume":"166","author":"Zeanah","year":"2009","journal-title":"Am. J. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0007","series-title":"United States Department of Agriculture, Economic Research Service","article-title":"Household Food Security in the United States in 2017","author":"Coleman-Jensen","year":"2018"},{"key":"10.1016\/j.physbeh.2020.113106_bib0008","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1111\/1467-8624.00469","article-title":"The environment of poverty: multiple stressor exposure, psychophysiological stress, and socioemotional adjustment","volume":"73","author":"Evans","year":"2002","journal-title":"Child Dev."},{"key":"10.1016\/j.physbeh.2020.113106_bib0009","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1037\/0002-9432.72.2.182","article-title":"Nutrition and brain development: social policy implications","volume":"72","author":"Tanner","year":"2002","journal-title":"Am. J. Orthopsychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0010","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/S0140-6736(07)61690-0","article-title":"Maternal and child undernutrition: global and regional exposures and health consequences","volume":"371","author":"Black","year":"2008","journal-title":"Lancet"},{"key":"10.1016\/j.physbeh.2020.113106_bib0011","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1067\/mpd.2000.106227","article-title":"Effects of growth restriction in early childhood on growth, IQ, and cognition at age 11 to 12 years and the benefits of nutritional supplementation and psychosocial stimulation","volume":"137","author":"Walker","year":"2000","journal-title":"J. Pediatr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0012","doi-asserted-by":"crossref","first-page":"590","DOI":"10.3390\/ijerph8020590","article-title":"Early postnatal protein-calorie malnutrition and cognition: a review of human and animal studies","volume":"8","author":"Laus","year":"2011","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"10.1016\/j.physbeh.2020.113106_bib0013","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1542\/peds.108.1.44","article-title":"insufficiency and American school-aged children's cognitive, academic, and psychosocial development","volume":"108","author":"Alaimo","year":"2001","journal-title":"Pediatrics"},{"key":"10.1016\/j.physbeh.2020.113106_bib0014","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1196\/annals.1425.001","article-title":"Food security, poverty, and human development in the United States","volume":"1136","author":"Cook","year":"2008","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0015","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.1176\/appi.ajp.161.11.2005","article-title":"Malnutrition at age 3 years and externalizing behavior problems at ages 8, 11, and 17 years","volume":"161","author":"Liu","year":"2004","journal-title":"Am. J. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0016","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1097\/01.mop.0000245360.13949.91","article-title":"The effect of childhood malnutrition on externalizing behavior","volume":"18","author":"Liu","year":"2006","journal-title":"Curr. Opin. Pediatr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0017","doi-asserted-by":"crossref","first-page":"389","DOI":"10.3390\/ijerph13040389","article-title":"Childhood reports of food neglect and impulse control problems and violence in adulthood","volume":"13","author":"Vaughn","year":"2016","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"10.1016\/j.physbeh.2020.113106_bib0018","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1203\/00006450-199009000-00018","article-title":"The long-term effects of early kwashiorkor compared with marasmus. IV. Performance on the national high school entrance examination","volume":"28","author":"Galler","year":"1990","journal-title":"Pediatr. Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0019","doi-asserted-by":"crossref","first-page":"1734","DOI":"10.1093\/ajcn\/30.10.1734","article-title":"Early malnutrition and ``late\u2019\u2019 adoption: a study of their effects on the development of Korean orphans adopted into American families","volume":"30","author":"Lien","year":"1977","journal-title":"Am. J. Clin. Nutr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0020","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1037\/neu0000058","article-title":"Neuropsychological outcomes at midlife following moderate to severe malnutrition in infancy","volume":"28","author":"Waber","year":"2014","journal-title":"Neuropsychology"},{"key":"10.1016\/j.physbeh.2020.113106_bib0021","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1111\/j.1469-7610.2010.02208.x","article-title":"Early childhood malnutrition predicts depressive symptoms at ages 11\u201317","volume":"51","author":"Galler","year":"2010","journal-title":"J. Child Psychol. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0022","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.jad.2012.11.029","article-title":"Depression and suicide ideation in late adolescence and early adulthood are an outcome of child hunger","volume":"150","author":"McIntyre","year":"2013","journal-title":"J. Affect. Disord."},{"key":"10.1016\/j.physbeh.2020.113106_bib0023","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1097\/DBP.0b013e31820b7707","article-title":"Cognitive impairment as a mediator in the developmental pathway from infant malnutrition to adolescent depressive symptoms in Barbadian youth","volume":"32","author":"Waber","year":"2011","journal-title":"J. Dev. Behav. Pediatr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0024","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1016\/j.biopsych.2007.05.012","article-title":"A longitudinal typology of symptoms of depression and anxiety over the life course","volume":"62","author":"Colman","year":"2007","journal-title":"Biol. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0025","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/0031-9384(92)90084-F","article-title":"Spatial learning ability of rats undernourished during early postnatal life","volume":"51","author":"Bedi","year":"1992","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0026","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1002\/dev.420200506","article-title":"Early-life malnutrition selectively retards the development of distal- but not proximal-cue navigation","volume":"20","author":"Castro","year":"1987","journal-title":"Dev. Psychobiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0027","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1016\/0163-1047(93)90580-B","article-title":"Impaired short-term memory resulting from postnatal undernutrition is attenuated by physostigmine","volume":"60","author":"Castro","year":"1993","journal-title":"Behav. Neural Biol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0028","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/S0166-4328(89)80058-0","article-title":"Early-life undernutrition impairs the development of the learning and short-term memory processes mediating performance in a conditional-spatial discrimination task","volume":"32","author":"Castro","year":"1989","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0029","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1016\/j.neubiorev.2010.10.017","article-title":"Maternal corticosterone effects on hypothalamus-pituitary-adrenal axis regulation and behavior of the offspring in rodents","volume":"35","author":"Catalani","year":"2011","journal-title":"Neurosci. Biobehav. Rev."},{"key":"10.1016\/j.physbeh.2020.113106_bib0030","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.bbr.2006.06.042","article-title":"Anxiolytic-like effects of short-term postnatal protein malnutrition in the elevated plus-maze test","volume":"173","author":"Francolin-Silva","year":"2006","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0031","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1038\/225468a0","article-title":"Effect of early malnutrition on the reaction of adult rats to aversive stimuli","volume":"225","author":"Levitsky","year":"1970","journal-title":"Nature"},{"key":"10.1016\/j.physbeh.2020.113106_bib0032","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/0031-9384(76)90188-8","article-title":"Passive avoidance behavior and response thresholds in adult male rats after early postnatal undernutrition","volume":"16","author":"Lynch","year":"1976","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0033","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1002\/dev.420050206","article-title":"Vulnerability of developing brain. IV. Passive avoidance behavior in young rats following maternal undernutrition","volume":"5","author":"Smart","year":"1972","journal-title":"Dev. Psychobiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0034","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/S0031-9384(01)00554-6","article-title":"Postnatal protein malnutrition affects play behavior and other social interactions in juvenile rats","volume":"74","author":"Almeida","year":"2001","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0035","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1016\/j.physbeh.2005.03.025","article-title":"Early postnatal protein malnutrition changes the development of social play in rats","volume":"85","author":"Maria Moreira Camargo","year":"2005","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0036","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1016\/S0899-9007(00)00431-7","article-title":"Long-term effects of severe undernutrition during the first year of life on brain development and learning in Chilean high-school graduates","volume":"16","author":"Ivanovic","year":"2000","journal-title":"Nutrition"},{"key":"10.1016\/j.physbeh.2020.113106_bib0037","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1203\/00006450-196903000-00010","article-title":"The effect of severe early malnutrition on cellular growth of human brain","volume":"3","author":"Winick","year":"1969","journal-title":"Pediatr. Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0038","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/0014-4886(71)90010-0","article-title":"Vulnerability of developing brain. VII. Permanent deficit of neurons in cerebral and cerebellar cortex following early mild undernutrition","volume":"32","author":"Dobbing","year":"1971","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0039","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1159\/000240430","article-title":"Vulnerability of developing brain. IX. The effect of nutritional growth retardation on the timing of the brain growth-spurt","volume":"19","author":"Dobbing","year":"1971","journal-title":"Biol. Neonate."},{"key":"10.1016\/j.physbeh.2020.113106_bib0040","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1093\/jn\/112.7.1362","article-title":"Effects of undernutrition at different ages early in life and later environmental complexity on parameters of the cerebrum and hippocampus in rats","volume":"112","author":"Katz","year":"1982","journal-title":"J. Nutr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0041","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1007\/BF01923346","article-title":"Early-life undernutrition causes deficits in rat dentate gyrus granule cell number","volume":"47","author":"Bedi","year":"1991","journal-title":"Experientia"},{"key":"10.1016\/j.physbeh.2020.113106_bib0042","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.neuroscience.2011.08.071","article-title":"Nutrient restriction during early life reduces cell proliferation in the hippocampus at adulthood but does not impair the neuronal differentiation process of the new generated cells","volume":"196","author":"Matos","year":"2011","journal-title":"Neuroscience"},{"key":"10.1016\/j.physbeh.2020.113106_bib0043","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/j.yebeh.2004.03.008","article-title":"Effect of food deprivation during early development on cognition and neurogenesis in the rat","volume":"5","author":"Akman","year":"2004","journal-title":"Epilepsy Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0044","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/S0166-4328(02)00010-4","article-title":"Early postnatal protein malnutrition affects learning and memory in the distal but not in the proximal cue version of the Morris water maze","volume":"133","author":"Fukuda","year":"2002","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0045","doi-asserted-by":"crossref","first-page":"e238","DOI":"10.1038\/tp.2013.7","article-title":"A role for synaptic plasticity in the adolescent development of executive function","volume":"3","author":"Selemon","year":"2013","journal-title":"Transl. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0046","doi-asserted-by":"crossref","first-page":"e1081","DOI":"10.1038\/tp.2017.48","article-title":"Stress and adolescent hippocampal neurogenesis: diet and exercise as cognitive modulators","volume":"7","author":"Hueston","year":"2017","journal-title":"Transl. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0047","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1038\/13158","article-title":"Brain development during childhood and adolescence: a longitudinal MRI study","volume":"2","author":"Giedd","year":"1999","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0048","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.pbb.2006.11.003","article-title":"Neurogenesis decreases during brain maturation from adolescence to adulthood","volume":"86","author":"He","year":"2007","journal-title":"Pharmacol. Biochem. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0049","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1002\/dneu.20987","article-title":"The pubertal-related decline in cellular proliferation and neurogenesis in the dentate gyrus of male rats is independent of the pubertal rise in gonadal hormones","volume":"72","author":"Ho","year":"2012","journal-title":"Dev. Neurobiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0050","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S0197-4580(03)00090-3","article-title":"Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation","volume":"25","author":"Heine","year":"2004","journal-title":"Neurobiol. Aging"},{"key":"10.1016\/j.physbeh.2020.113106_bib0051","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1016\/j.neuroscience.2009.06.057","article-title":"Prozac during puberty: distinctive effects on neurogenesis as a function of age and sex","volume":"163","author":"Hodes","year":"2009","journal-title":"Neuroscience"},{"key":"10.1016\/j.physbeh.2020.113106_bib0052","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.neuroscience.2017.09.020","article-title":"Adolescent social isolation stress unmasks the combined effects of adolescent exercise and adult inflammation on hippocampal neurogenesis and behavior","volume":"365","author":"Hueston","year":"2017","journal-title":"Neuroscience"},{"key":"10.1016\/j.physbeh.2020.113106_bib0053","doi-asserted-by":"crossref","first-page":"1988","DOI":"10.1038\/sj.npp.1300528","article-title":"Delayed effects of early stress on hippocampal development","volume":"29","author":"Andersen","year":"2004","journal-title":"Neuropsychopharmacology"},{"key":"10.1016\/j.physbeh.2020.113106_bib0054","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.dcn.2016.10.004","article-title":"Sensitive periods of substance abuse: early risk for the transition to dependence","volume":"25","author":"Jordan","year":"2017","journal-title":"Dev. Cogn. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0055","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.brainres.2016.03.021","article-title":"The impact of stress on the structure of the adolescent brain: implications for adolescent mental health","volume":"1654","author":"Romeo","year":"2017","journal-title":"Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0056","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1001\/archpsyc.62.6.593","article-title":"Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication","volume":"62","author":"Kessler","year":"2005","journal-title":"Arch. Gen. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0057","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1186\/1471-244X-2-3","article-title":"The influence of age on the female\/male ratio of treated incidence rates in depression","volume":"2","author":"Gutierrez-Lobos","year":"2002","journal-title":"BMC Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0058","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1037\/0021-843X.107.1.128","article-title":"Development of depression from preadolescence to young adulthood: emerging gender differences in a 10-year longitudinal study","volume":"107","author":"Hankin","year":"1998","journal-title":"J. Abnorm. Psychol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0059","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1002\/cne.902180310","article-title":"The comparative effects of early-life undernutrition and subsequent differential environments on the dendritic branching of pyramidal cells in rat visual cortex","volume":"218","author":"Davies","year":"1983","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0060","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1016\/0091-3057(90)90113-V","article-title":"Decreased reactivity to anxiolytics caused by early protein malnutrition in rats","volume":"36","author":"Almeida","year":"1990","journal-title":"Pharmacol. Biochem. Behav."},{"issue":"41 Suppl","key":"10.1016\/j.physbeh.2020.113106_bib0061","first-page":"S48","article-title":"Malnutrition increases dentate granule cell proliferation in immature rats after status epilepticus","volume":"6","author":"Nunes","year":"2000","journal-title":"Epilepsia"},{"key":"10.1016\/j.physbeh.2020.113106_bib0062","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1016\/S0003-3472(73)80024-7","article-title":"Maternal behavior of undernourished mother rats","volume":"21","author":"Smart","year":"1973","journal-title":"Anim. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0063","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/0031-9384(95)00065-Q","article-title":"Nutritional status and behavior during lactation","volume":"58","author":"Pachon","year":"1995","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0064","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1016\/0031-9384(95)02018-7","article-title":"Rasmussen, K. M. Food restriction, gonadotropins, and behavior in the lactating rat","volume":"58","author":"McGuire","year":"1995","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0065","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1644\/13-MAMM-A-060.1","article-title":"Food restriction affects the maternal behavior provided by female meadow voles (Microtus pennsylvanicus)","volume":"94","author":"Sabau","year":"2013","journal-title":"J. Mammal."},{"key":"10.1016\/j.physbeh.2020.113106_bib0066","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1002\/dev.420070607","article-title":"Protein malnutrition in the rat: its effects on maternal behavior and pup development","volume":"7","author":"Massaro","year":"1974","journal-title":"Dev. Psychobiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0067","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1590\/S0100-879X1999000800007","article-title":"Ethological analysis of mother-pup interactions and other behavioral reactions in rats: effects of malnutrition and tactile stimulation of the pups","volume":"32","author":"Riul","year":"1999","journal-title":"Braz. J. Med. Biol. Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0068","doi-asserted-by":"crossref","first-page":"3091","DOI":"10.1111\/j.1460-9568.2007.05522.x","article-title":"Long-term behavioural and molecular alterations associated with maternal separation in rats","volume":"25","author":"Lippmann","year":"2007","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0069","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/S0306-4530(01)00019-1","article-title":"long maternal separations in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety","volume":"26","author":"Boccia","year":"2001","journal-title":"Psychoneuroendocrinology"},{"key":"10.1016\/j.physbeh.2020.113106_bib0070","first-page":"8","article-title":"The behavioral and immunological impact of maternal separation: a matter of timing","author":"Roque","year":"2014","journal-title":"Front. Behav. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0071","doi-asserted-by":"crossref","first-page":"21","DOI":"10.3389\/fpsyt.2011.00021","article-title":"Litter gender composition and sex affect maternal behavior and DNA methylation levels of the oprm1 gene in rat offspring","volume":"2","author":"Hao","year":"2011","journal-title":"Front. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0072","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1037\/h0077599","article-title":"Mother rats interact differently with male and female offspring","volume":"93","author":"Moore","year":"1979","journal-title":"J. Comp. Physiol. Psychol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0073","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.bbr.2018.07.012","article-title":"High nursing demand reduces depression-like behavior despite increasing glucocorticoid concentrations and reducing hippocampal neurogenesis in late postpartum rats","volume":"353","author":"De Guzman","year":"2018","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0074","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/cne.10874","article-title":"Transient expression of doublecortin during adult neurogenesis","volume":"467","author":"Brown","year":"2003","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0075","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1460-9568.2004.03813.x","article-title":"Doublecortin expression levels in adult brain reflect neurogenesis","volume":"21","author":"Couillard-Despres","year":"2005","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0076","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1037\/0033-2909.83.3.482","article-title":"The open-field test: a critical review","volume":"83","author":"Walsh","year":"1976","journal-title":"Psychol. Bull."},{"key":"10.1016\/j.physbeh.2020.113106_bib0077","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1038\/266730a0","article-title":"Depression a new animal model sensitive to antidepressant treatments","volume":"266","author":"Porsolt","year":"1977","journal-title":"Nature"},{"key":"10.1016\/j.physbeh.2020.113106_bib0078","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/j.neuroscience.2013.08.017","article-title":"Neurogenesis along the septo-temporal axis of the hippocampus: are depression and the action of antidepressants region-specific?","volume":"252","author":"Tanti","year":"2013","journal-title":"Neuroscience"},{"key":"10.1016\/j.physbeh.2020.113106_bib0079","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1111\/j.1365-2818.1987.tb02837.x","article-title":"The efficiency of systematic sampling in stereology and its prediction","volume":"147","author":"Gundersen","year":"1987","journal-title":"J. Microsc."},{"key":"10.1016\/j.physbeh.2020.113106_bib0080","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/0014-2999(78)90118-8","article-title":"Behavioural despair in rats: a new model sensitive to antidepressant treatments","volume":"47","author":"Porsolt","year":"1978","journal-title":"Eur. J. Pharmacol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0081","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1037\/1064-1297.5.2.107","article-title":"Acute and chronic antidepressant drug treatment in the rat forced swimming test model of depression","volume":"5","author":"Detke","year":"1997","journal-title":"Exp. Clin. Psychopharmacol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0082","doi-asserted-by":"crossref","DOI":"10.1155\/2016\/6503162","article-title":"Coping with the forced swim stressor: towards understanding an adaptive mechanism","volume":"2016","author":"de Kloet","year":"2016","journal-title":"Neural Plast."},{"key":"10.1016\/j.physbeh.2020.113106_bib0083","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.psyneuen.2015.08.028","article-title":"Immobility in the forced swim test is adaptive and does not reflect depression","volume":"62","author":"Molendijk","year":"2015","journal-title":"Psychoneuroendocrinology"},{"key":"10.1016\/j.physbeh.2020.113106_bib0084","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1016\/0031-9384(92)90308-O","article-title":"Effects of early postnatal malnutrition and chlordiazepoxide on experimental aversive situations","volume":"51","author":"Almeida","year":"1992","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0085","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1111\/brv.12210","article-title":"Effect of maternal diet on offspring coping styles in rodents: a systematic review and meta-analysis","volume":"91","author":"Besson","year":"2016","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"10.1016\/j.physbeh.2020.113106_bib0086","first-page":"1216","article-title":"Behavioural effects of prenatal and postnatal undernutrition in rats","volume":"34","author":"Jaiswal","year":"1996","journal-title":"Indian J. Exp. Biol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0087","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.ijdevneu.2011.10.002","article-title":"Maternal protein restriction in the rat during pregnancy and\/or lactation alters cognitive and anxiety behaviors of female offspring","volume":"30","author":"Reyes-Castro","year":"2012","journal-title":"Int. J. Dev. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0088","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.physbeh.2014.05.032","article-title":"Tests of unconditioned anxiety - pitfalls and disappointments","volume":"135","author":"Ennaceur","year":"2014","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0089","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/S0166-4328(01)00291-1","article-title":"Measuring normal and pathological anxiety-like behaviour in mice: a review","volume":"125","author":"Belzung","year":"2001","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0090","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1038\/nn.4112","article-title":"Sex differences and stress across the lifespan","volume":"18","author":"Bale","year":"2015","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0091","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1126\/science.6163211","article-title":"Sexual differentiation of the central nervous system","volume":"211","author":"MacLusky","year":"1981","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2020.113106_bib0092","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1126\/science.175.4017.82","article-title":"Prenatal stress feminizes and demasculinizes the behavior of males","volume":"175","author":"Ward","year":"1972","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2020.113106_bib0093","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/0031-9384(91)90552-Y","article-title":"Prenatal stress feminizes juvenile play patterns in male rats","volume":"50","author":"Ward","year":"1991","journal-title":"Physiol. Behav."},{"issue":"Suppl 3","key":"10.1016\/j.physbeh.2020.113106_bib0094","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1289\/ehp.00108s3511","article-title":"Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models","volume":"108","author":"Rice","year":"2000","journal-title":"Environ. Health Perspect."},{"key":"10.1016\/j.physbeh.2020.113106_bib0095","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1002\/cne.903010304","article-title":"Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods","volume":"301","author":"Altman","year":"1990","journal-title":"J. Comp. Neurol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0096","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1016\/j.yhbeh.2006.04.008","article-title":"High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression","volume":"50","author":"Brummelte","year":"2006","journal-title":"Horm. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0097","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1002\/dneu.20805","article-title":"Elevated corticosterone levels in stomach milk, serum, and brain of male and female offspring after maternal corticosterone treatment in the rat","volume":"70","author":"Brummelte","year":"2010","journal-title":"Dev. Neurobiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0098","doi-asserted-by":"crossref","first-page":"3845","DOI":"10.1523\/JNEUROSCI.3609-06.2007","article-title":"GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states","volume":"27","author":"Earnheart","year":"2007","journal-title":"J. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0099","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1037\/h0077560","article-title":"Modulation of behavioral inhibition in appetitive extinction following manipulation of adrenal steroids in rats: implications for involvement of the hippocampus","volume":"93","author":"Micco","year":"1979","journal-title":"J. Comp. Physiol. Psychol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0100","doi-asserted-by":"crossref","first-page":"2368","DOI":"10.1038\/npp.2015.85","article-title":"Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors","volume":"40","author":"Hill","year":"2015","journal-title":"Neuropsychopharmacology"},{"key":"10.1016\/j.physbeh.2020.113106_bib0101","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/S0361-9230(96)00214-6","article-title":"Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus","volume":"41","author":"Debassio","year":"1996","journal-title":"Brain Res. Bull."},{"key":"10.1016\/j.physbeh.2020.113106_bib0102","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/s13293-017-0142-x","article-title":"Sex-dependent effects of maternal corticosterone and SSRI treatment on hippocampal neurogenesis across development","volume":"8","author":"Gobinath","year":"2017","journal-title":"Biol. Sex Differ."},{"key":"10.1016\/j.physbeh.2020.113106_bib0103","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.brainres.2008.06.059","article-title":"Age-dependent decline in hippocampal neurogenesis is not altered by chronic treatment with fluoxetine","volume":"1228","author":"Cowen","year":"2008","journal-title":"Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0104","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1016\/j.cell.2013.05.002","article-title":"Dynamics of hippocampal neurogenesis in adult humans","volume":"153","author":"Spalding","year":"2013","journal-title":"Cell"},{"key":"10.1016\/j.physbeh.2020.113106_bib0105","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1093\/jn\/103.9.1327","article-title":"Vulnerability of developing brain: relative effects of growth restriction during the fetal and suckling periods on behavior and brain composition of adult rats","volume":"103","author":"Smart","year":"1973","journal-title":"J. Nutr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0106","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1038\/mp.2011.48","article-title":"Antidepressants recruit new neurons to improve stress response regulation","volume":"16","author":"Surget","year":"2011","journal-title":"Mol. Psychiatry."},{"key":"10.1016\/j.physbeh.2020.113106_bib0107","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1126\/science.1083328","article-title":"Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants","volume":"301","author":"Santarelli","year":"2003","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2020.113106_bib0108","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1038\/mp.2009.15","article-title":"Adult hippocampal neurogenesis is involved in anxiety-related behaviors","volume":"14","author":"Revest","year":"2009","journal-title":"Mol. Psychiatry"},{"key":"10.1016\/j.physbeh.2020.113106_bib0109","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1038\/nature10287","article-title":"Adult hippocampal neurogenesis buffers stress responses and depressive behaviour","volume":"476","author":"Snyder","year":"2011","journal-title":"Nature"},{"key":"10.1016\/j.physbeh.2020.113106_bib0110","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1126\/science.1248903","article-title":"Hippocampal neurogenesis regulates forgetting during adulthood and infancy","volume":"344","author":"Akers","year":"2014","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2020.113106_bib0111","doi-asserted-by":"crossref","first-page":"57","DOI":"10.3389\/fnins.2013.00057","article-title":"Hippocampus-dependent learning influences hippocampal neurogenesis","volume":"7","author":"Epp","year":"2013","journal-title":"Front. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0112","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1038\/nrn2822","article-title":"New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?","volume":"11","author":"Deng","year":"2010","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.physbeh.2020.113106_bib0113","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1016\/0031-9384(89)90210-2","article-title":"The effects of undernutrition during early life on spatial learning","volume":"45","author":"Campbell","year":"1989","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0114","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1002\/hipo.22374","article-title":"Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice","volume":"25","author":"Naninck","year":"2015","journal-title":"Hippocampus"},{"key":"10.1016\/j.physbeh.2020.113106_bib0115","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1093\/jn\/96.3.375","article-title":"Effect of undernutrition on the size and composition of the rat brain","volume":"96","author":"Culley","year":"1968","journal-title":"J. Nutr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0116","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1079\/BJN19820083","article-title":"The effect of early postnatal undernutrition on the growth and development of the rat brain","volume":"48","author":"Morgan","year":"1982","journal-title":"Br. J. Nutr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0117","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.bbr.2005.03.008","article-title":"Effects of different malnutrition techniques on the behavior of rats tested in the elevated T-maze","volume":"162","author":"Hernandes","year":"2005","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0118","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.brainres.2007.01.109","article-title":"Undernutrition during early life increases the level of apoptosis in the dentate gyrus but not in the CA2+CA3 region of the hippocampal formation","volume":"1143","author":"Jahnke","year":"2007","journal-title":"Brain. Res."},{"key":"10.1016\/j.physbeh.2020.113106_bib0119","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.physbeh.2008.05.021","article-title":"Neonatal food restriction permanently alters rat body dimensions and energy intake","volume":"95","author":"Remmers","year":"2008","journal-title":"Physiol. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0120","doi-asserted-by":"crossref","first-page":"16757","DOI":"10.1073\/pnas.1012911107","article-title":"The Dutch Hunger Winter and the developmental origins of health and disease","volume":"107","author":"Schulz","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.physbeh.2020.113106_bib0121","first-page":"341","article-title":"Low birth weight and obesity: causal or casual association?","volume":"33","author":"Ribeiro","year":"2015","journal-title":"Rev. Paul. Pediatr."},{"key":"10.1016\/j.physbeh.2020.113106_bib0122","doi-asserted-by":"crossref","first-page":"R91","DOI":"10.1152\/ajpregu.00340.2004","article-title":"Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition","volume":"288","author":"Desai","year":"2005","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0123","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1113\/jphysiol.2005.100313","article-title":"A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat","volume":"571","author":"Zambrano","year":"2006","journal-title":"J. Physiol."},{"key":"10.1016\/j.physbeh.2020.113106_bib0124","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1016\/S0091-3057(99)00139-2","article-title":"Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety","volume":"64","author":"Fernandes","year":"1999","journal-title":"Pharmacol. Biochem. Behav."},{"key":"10.1016\/j.physbeh.2020.113106_bib0125","first-page":"4","article-title":"Sexually divergent expression of active and passive conditioned fear responses in rats","author":"Gruene","year":"2015","journal-title":"eLife."},{"key":"10.1016\/j.physbeh.2020.113106_bib0126","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1016\/j.nbd.2012.02.014","article-title":"Neonatal testosterone partially organizes sex differences in stress-induced emotionality in mice","volume":"46","author":"Seney","year":"2012","journal-title":"Neurobiol. Dis."},{"key":"10.1016\/j.physbeh.2020.113106_bib0127","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1002\/j.2040-4603.2014.tb00575.x","article-title":"Sex differences in the HPA axis","volume":"4","author":"Goel","year":"2014","journal-title":"Compr. Physiol."}],"container-title":["Physiology &amp; Behavior"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938420304200?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938420304200?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,21]],"date-time":"2025-09-21T18:16:05Z","timestamp":1758478565000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0031938420304200"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10]]},"references-count":127,"alternative-id":["S0031938420304200"],"URL":"https:\/\/doi.org\/10.1016\/j.physbeh.2020.113106","relation":{},"ISSN":["0031-9384"],"issn-type":[{"type":"print","value":"0031-9384"}],"subject":[],"published":{"date-parts":[[2020,10]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Rotated nursing environment with underfeeding: A form of early-life adversity with sex- and age-dependent effects on coping behavior and hippocampal neurogenesis","name":"articletitle","label":"Article Title"},{"value":"Physiology & Behavior","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.physbeh.2020.113106","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2020 Published by Elsevier Inc.","name":"copyright","label":"Copyright"}],"article-number":"113106"}}