{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T13:35:03Z","timestamp":1790775303913,"version":"4.1.0"},"reference-count":74,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2018,10,17]],"date-time":"2018-10-17T00:00:00Z","timestamp":1539734400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Research Deputy of School of Medicine, Shahid Beheshti University of Medical Sciences","award":["[Grant Number: 13\/740]"],"award-info":[{"award-number":["[Grant Number: 13\/740]"]}]},{"name":"Neurophysiology research center, Shahid Beheshti University of Medical Sciences","award":["[Grant Number: 35]"],"award-info":[{"award-number":["[Grant Number: 35]"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0204731","type":"journal-article","created":{"date-parts":[[2018,10,17]],"date-time":"2018-10-17T18:47:45Z","timestamp":1539802065000},"page":"e0204731","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":36,"title":["Maternal separation blunted spatial memory formation independent of peripheral and hippocampal insulin content in young adult male rats"],"prefix":"10.1371","volume":"13","author":[{"given":"Soheila","family":"Maghami","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8307-1848","authenticated-orcid":true,"given":"Homeira","family":"Zardooz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fariba","family":"Khodagholi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fatemeh","family":"Binayi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roya","family":"Ranjbar Saber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mehdi","family":"Hedayati","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hedayat","family":"Sahraei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammad Ali","family":"Ansari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2018,10,17]]},"reference":[{"issue":"1","key":"ref1","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s00213-010-2009-2","article-title":"Effects of early life stress on cognitive and affective function: an integrated review of human literature","volume":"214","author":"P Pechtel","year":"2011","journal-title":"Psychopharmacology"},{"issue":"4","key":"ref2","doi-asserted-by":"crossref","first-page":"1705","DOI":"10.1016\/j.neuroscience.2010.06.035","article-title":"Early stress exposure impairs synaptic potentiation in the rat medial prefrontal cortex underlying contextual fear extinction","volume":"169","author":"C Judo","year":"2010","journal-title":"Neuroscience"},{"key":"ref3","first-page":"2007","article-title":"Stress and memory: behavioral effects and neurobiological mechanisms","author":"C Sandi","year":"2007","journal-title":"Neural plast"},{"issue":"8","key":"ref4","doi-asserted-by":"crossref","first-page":"1664","DOI":"10.1038\/npp.2010.13","article-title":"Interactions between age, stress and insulin on cognition: implications for Alzheimer's disease","volume":"35","author":"M Solas","year":"2010","journal-title":"Neuropsychopharmacology"},{"issue":"7","key":"ref5","doi-asserted-by":"crossref","first-page":"1680","DOI":"10.1016\/j.neurobiolaging.2014.01.024","article-title":"Maternal separation impairs long term-potentiation in CA1-CA3 synapses and hippocampal-dependent memory in old rats","volume":"35","author":"VC Sousa","year":"2014","journal-title":"Neurobiol aging"},{"issue":"7","key":"ref6","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1016\/j.neubiorev.2011.07.002","article-title":"Stress effects on memory: an update and integration","volume":"36","author":"L Schwabe","year":"2012","journal-title":"Neurosci Biobehav Rev"},{"issue":"3","key":"ref7","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.pedneo.2011.03.008","article-title":"Effects of early life stress on neuroendocrine and neurobehavior: mechanisms and implications","volume":"52","author":"M-C Lai","year":"2011","journal-title":"Pediatr Neonatol"},{"issue":"9","key":"ref8","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1016\/j.nut.2016.02.016","article-title":"Prolonged maternal separation induces undernutrition and systemic inflammation with disrupted hippocampal development in mice","volume":"32","author":"IL Figueiredo","year":"2016","journal-title":"Nutrition"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.bbr.2013.03.040","article-title":"Early maternal separation: neurobehavioral consequences in mother rats","volume":"248","author":"JP Aguggia","year":"2013","journal-title":"Behav Brain Res"},{"key":"ref10","doi-asserted-by":"crossref","DOI":"10.1155\/2012\/384017","article-title":"Insulin in central nervous system: more than just a peripheral hormone","volume":"2012","author":"AI Duarte","year":"2012","journal-title":"J aging res"},{"issue":"10","key":"ref11","doi-asserted-by":"crossref","first-page":"1326","DOI":"10.1016\/j.psyneuen.2004.04.003","article-title":"Intranasal insulin improves memory in humans","volume":"29","author":"C Benedict","year":"2004","journal-title":"Psychoneuroendocrinology"},{"issue":"2","key":"ref12","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1016\/j.bbr.2006.10.011","article-title":"Insulin protects against stress-induced impairments in water maze performance","volume":"176","author":"M Moosavi","year":"2007","journal-title":"Behav brain res"},{"issue":"49","key":"ref13","doi-asserted-by":"crossref","first-page":"34893","DOI":"10.1074\/jbc.274.49.34893","article-title":"Brain insulin receptors and spatial memory correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats","volume":"274","author":"W Zhao","year":"1999","journal-title":"J Biol Chem"},{"issue":"1","key":"ref14","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1001\/archneurol.2011.233","article-title":"Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial","volume":"69","author":"S Craft","year":"2012","journal-title":"Arch neurol"},{"issue":"20","key":"ref15","doi-asserted-by":"crossref","first-page":"11056","DOI":"10.1073\/pnas.97.20.11056","article-title":"Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress","volume":"97","author":"AM Magari\u00f1os","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"1","key":"ref16","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/s12986-017-0177-3","article-title":"Maternal high-fat diet intensifies the metabolic response to stress in male rat offspring","volume":"14","author":"R Karbaschi","year":"2017","journal-title":"Nutr Metab"},{"key":"ref17","first-page":"163","article-title":"Effects of acute and chronic psychological stress on isolated islets' insulin release","volume":"11","author":"H Zardooz","year":"2012","journal-title":"EXCLI J"},{"issue":"2","key":"ref18","doi-asserted-by":"crossref","first-page":"123","DOI":"10.3109\/10253890903080379","article-title":"Chronic exogenous corticosterone administration generates an insulin-resistant brain state in rats","volume":"13","author":"J Osmanovic","year":"2010","journal-title":"Stress"},{"issue":"5","key":"ref19","doi-asserted-by":"crossref","first-page":"2503","DOI":"10.1210\/endo-129-5-2503","article-title":"Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat","volume":"129","author":"V Viau","year":"1991","journal-title":"Endocrinology"},{"issue":"Suppl","key":"ref20","doi-asserted-by":"crossref","first-page":"E38","DOI":"10.1111\/j.1749-6632.2010.05568.x","article-title":"Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling","volume":"1204","author":"BS McEwen","year":"2010","journal-title":"Ann N Y Acad Sci"},{"issue":"4","key":"ref21","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/S0149-7634(00)00014-2","article-title":"The adolescent brain and age-related behavioral manifestations","volume":"24","author":"L.P. Spear","year":"2000","journal-title":"Neurosci Biobehav Rev"},{"issue":"3","key":"ref22","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1111\/j.1440-1681.2007.04576.x","article-title":"Role of dorsal hippocampal cannabinoid receptors and nitric oxide in anxiety like behaviors in rats using the elevated plus-maze test","volume":"34","author":"A Roohbakhsh","year":"2007","journal-title":"Clin Exp Pharmacol Physiol"},{"key":"ref23","article-title":"The forced swim test as a model of depressive-like behavior","volume":"97","author":"R Yankelevitch-Yahav","year":"2015","journal-title":"J Vis Exp"},{"issue":"1","key":"ref24","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1037\/h0077579","article-title":"Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat","volume":"93","author":"CA Barnes","year":"1979","journal-title":"J Comp Physiol Psychol"},{"issue":"5","key":"ref25","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1016\/S0031-9384(97)00529-5","article-title":"Chronic corticosterone impairs memory performance in the Barnes maze","volume":"63","author":"RN McLay","year":"1998","journal-title":"Physiol Behav"},{"issue":"2","key":"ref26","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1101\/lm.028076.112","article-title":"Optimization of apparatus design and behavioral measures for the assessment of visuo-spatial learning and memory of mice on the Barnes maze","volume":"20","author":"TP O'Leary","year":"2013","journal-title":"Learn Mem"},{"issue":"6","key":"ref27","first-page":"973","article-title":"Plasma corticosterone, insulin and glucose changes induced by brief exposure to isoflurane, diethyl ether and CO2 in male rats","volume":"59","author":"H Zardooz","year":"2010","journal-title":"Physiol Res"},{"issue":"1","key":"ref28","doi-asserted-by":"crossref","first-page":"35","DOI":"10.2337\/diab.16.1.35","article-title":"Method for the isolation of intact islets of Langerhans from the rat pancreas","volume":"16","author":"PE Lacy","year":"1967","journal-title":"Diabetes"},{"key":"ref29","first-page":"653","article-title":"High-fat diet with stress impaired islets\u2019insulin secretion by reducing plasma estradiol and pancreatic glut2 protein levels in rats\u2019proestrus phase","volume":"67","author":"M Salimi","year":"2016","journal-title":"J Physiol Pharmacol"},{"key":"ref30","article-title":"The rat brain in stereotaxic coordinates","author":"G Paxinos","year":"2007"},{"issue":"5","key":"ref31","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1007\/s11064-011-0417-2","article-title":"Dietary supplementation with tBHQ, an Nrf2 stabilizer molecule, confers neuroprotection against apoptosis in amyloid \u03b2-injected rat","volume":"36","author":"F Nouhi","year":"2011","journal-title":"Neurochem Res"},{"issue":"3","key":"ref32","doi-asserted-by":"crossref","first-page":"394","DOI":"10.55782\/ane-2013-1946","article-title":"Long-term effects of the maternal deprivation on the volume and number of neurons in the rat neocortex and hippocampus","volume":"73","author":"M Aksic","year":"2013","journal-title":"Acta Neurobiol Exp (Wars)"},{"issue":"2","key":"ref33","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.ijdevneu.2009.12.005","article-title":"Prolonged maternal separation decreases granule cell number in the dentate gyrus of 3-week-old male rats","volume":"28","author":"S Oreland","year":"2010","journal-title":"Int J Dev Neurosci"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.nlm.2013.06.012","article-title":"Spatial memory impairment and changes in hippocampal morphology are triggered by high-fat diets in adolescent mice. Is there a role of leptin?","volume":"106","author":"I Valladolid-Acebes","year":"2013","journal-title":"Neurobiol Learn Mem"},{"issue":"6","key":"ref35","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1038\/nrn849","article-title":"The stressed hippocampus, synaptic plasticity and lost memories","volume":"3","author":"JJ Kim","year":"2002","journal-title":"Nat Rev Neurosci"},{"issue":"3","key":"ref36","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1007\/BF01852291","article-title":"Effects of early undernutrition on hippocampal development and function","volume":"180","author":"TC Jordan","year":"1982","journal-title":"Res Exp Med (Berl)"},{"issue":"22","key":"ref37","doi-asserted-by":"crossref","first-page":"7208","DOI":"10.1523\/JNEUROSCI.6068-08.2009","article-title":"Rat prefrontal cortical neurons selectively code strategy switches","volume":"29","author":"EL Rich","year":"2009","journal-title":"Journal of Neuroscience"},{"issue":"1","key":"ref38","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1037\/0735-7044.113.1.32","article-title":"Involvement of rodent prefrontal cortex subregions in strategy switching","volume":"113","author":"ME Ragozzino","year":"1999","journal-title":"Behavioral neuroscience"},{"issue":"6","key":"ref39","doi-asserted-by":"crossref","first-page":"1462","DOI":"10.1016\/S1734-1140(13)71506-8","article-title":"Impact of early-life stress on the medial prefrontal cortex functions\u2013a search for the pathomechanisms of anxiety and mood disorders","volume":"65","author":"A Chocyk","year":"2013","journal-title":"Pharmacological Reports"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.neuroscience.2018.03.038","article-title":"Previous Early-life Stress Modifies Acute Corticosterone-induced Synaptic Plasticity in the Medial Prefrontal Cortex of Adolescent Rats","volume":"379","author":"I Majcher-Ma\u015blanka","year":"2018","journal-title":"Neuroscience"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.bbr.2016.08.055","article-title":"Behavioral effects of chronically elevated corticosterone in subregions of the medial prefrontal cortex","volume":"316","author":"JD Croteau","year":"2017","journal-title":"Behavioural brain research"},{"issue":"5","key":"ref42","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1002\/dev.21130","article-title":"The timing of maternal separation affects Morris water maze performance and long\u2010term potentiation in male rats","volume":"56","author":"X Cao","year":"2014","journal-title":"Developmental psychobiology"},{"issue":"9","key":"ref43","doi-asserted-by":"crossref","first-page":"1985","DOI":"10.1016\/j.neubiorev.2012.07.003","article-title":"Early life manipulations alter learning and memory in rats","volume":"36","author":"TA Kosten","year":"2012","journal-title":"Neuroscience & Biobehavioral Reviews"},{"issue":"1","key":"ref44","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.joto.2015.07.001","article-title":"Spatial learning and memory deficits in young adult mice exposed to a brief intense noise at postnatal age","volume":"10","author":"S Tao","year":"2015","journal-title":"Journal of otology"},{"issue":"6","key":"ref45","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1038\/nrn2651","article-title":"Stress, memory and the amygdala","volume":"10","author":"B Roozendaal","year":"2009","journal-title":"Nature Rev Neurosci"},{"issue":"3","key":"ref46","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1046\/j.1460-9568.2003.02479.x","article-title":"Sex differences in anxiety, sensorimotor gating and expression of the \u03b14 subunit of the GABAA receptor in the amygdala after progesterone withdrawal","volume":"17","author":"M Gulinello","year":"2003","journal-title":"Eur J Neurosci"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.psyneuen.2014.01.014","article-title":"Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats","volume":"42","author":"M Crumeyrolle-Arias","year":"2014","journal-title":"Psychoneuroendocrinology"},{"issue":"1","key":"ref48","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1203\/01.pdr.0000190577.62426.45","article-title":"Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance","volume":"59","author":"MG Gareau","year":"2006","journal-title":"Pediatr Res"},{"issue":"3pt1","key":"ref49","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1016\/S0022-5347(05)00321-6","article-title":"Maternal separation uncouples reflex from spontaneous voiding in rat pups","volume":"175","author":"HY Wu","year":"2006","journal-title":"J Urol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.bbr.2016.04.031","article-title":"Developmental and behavioral consequences of early life maternal separation stress in a mouse model of fetal alcohol spectrum disorder","volume":"308","author":"B Alberry","year":"2016","journal-title":"Behav Brain Res"},{"issue":"39","key":"ref51","doi-asserted-by":"crossref","first-page":"13005","DOI":"10.1523\/JNEUROSCI.1784-10.2010","article-title":"Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors","volume":"30","author":"AS Ivy","year":"2010","journal-title":"J Neurosci"},{"key":"ref52","doi-asserted-by":"crossref","DOI":"10.3389\/fnbeh.2014.00136","article-title":"Learning and memory impairments in a neuroendocrine mouse model of anxiety\/depression","volume":"8","author":"F Darcet","year":"2014","journal-title":"Front Behav Neurosci"},{"issue":"1","key":"ref53","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1113\/jphysiol.2006.105254","article-title":"Fetal programming of hypothalamo\u2010pituitary\u2010adrenal function: prenatal stress and glucocorticoids","volume":"572","author":"A Kapoor","year":"2006","journal-title":"J physiol"},{"issue":"2","key":"ref54","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1046\/j.0007-1331.2001.00753.x","article-title":"Perinatal malnutrition programs sympathoadrenal and hypothalamic-pituitary-adrenal axis responsiveness to restraint stress in adult male rats","volume":"14","author":"J Lesage","year":"2002","journal-title":"J Neuroendocrinol"},{"issue":"2","key":"ref55","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/j.neuroscience.2005.08.089","article-title":"Early life trauma decreases glucocorticoid receptors in rat dentate gyrus upon adult re-stress: reversal by escitalopram","volume":"137","author":"J Uys","year":"2006","journal-title":"Neuroscience"},{"issue":"3","key":"ref56","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.yfrne.2005.10.002","article-title":"Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat","volume":"26","author":"M Szyf","year":"2005","journal-title":"Front Neuroendocrinol"},{"issue":"1","key":"ref57","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1023\/B:MEBR.0000027413.42946.61","article-title":"The effects of repeated intra-amygdala CRF injections on rat behavior and HPA axis function after stress","volume":"19","author":"W Daniels","year":"2004","journal-title":"Metab Brain Dis"},{"issue":"1","key":"ref58","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1023\/B:MEBR.0000027412.19664.b3","article-title":"Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor","volume":"19","author":"W Daniels","year":"2004","journal-title":"Metab Brain Dis"},{"issue":"1","key":"ref59","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1196\/annals.1364.060","article-title":"Developmental trauma is associated with behavioral hyperarousal, altered HPA axis activity, and decreased hippocampal neurotrophin expression in the adult rat","volume":"1071","author":"JD Uys","year":"2006","journal-title":"Ann N Y Acad Sci"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.psyneuen.2014.01.009","article-title":"Early life maternal separation stress augmentation of limbic epileptogenesis: the role of corticosterone and HPA axis programming","volume":"42","author":"AS Koe","year":"2014","journal-title":"Psychoneuroendocrinology"},{"issue":"4","key":"ref61","doi-asserted-by":"crossref","first-page":"e62031","DOI":"10.1371\/journal.pone.0062031","article-title":"Early life stress interacts with the diet deficiency of omega-3 fatty acids during the life course increasing the metabolic vulnerability in adult rats","volume":"8","author":"JR Bernardi","year":"2013","journal-title":"PLoS One"},{"issue":"4","key":"ref62","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1007\/s11011-008-9102-9","article-title":"Neonatal maternal separation affects endocrine and metabolic stress responses to ether exposure but not to restraint exposure in adult rats","volume":"23","author":"DRC F\u00f3scolo","year":"2008","journal-title":"Metab Brain Dis"},{"issue":"2","key":"ref63","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1007\/s12020-014-0337-4","article-title":"Effect of early life stress on pancreatic isolated islets' insulin secretion in young adult male rats subjected to chronic stress","volume":"48","author":"F Sadeghimahalli","year":"2015","journal-title":"Endocrine"},{"issue":"7","key":"ref64","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1002\/dmrr.2310","article-title":"Effects of glucocorticoids and exercise on pancreatic \u03b2\u2010cell function and diabetes development","volume":"28","author":"JL Beaudry","year":"2012","journal-title":"Diabetes Metab Res Rev"},{"issue":"18","key":"ref65","doi-asserted-by":"crossref","first-page":"e12972","DOI":"10.14814\/phy2.12972","article-title":"Sex differences in adult rat insulin and glucose responses to arginine: programming effects of neonatal separation, hypoxia, and hypothermia","volume":"4","author":"AL Gehrand","year":"2016","journal-title":"Physiol Rep"},{"issue":"6","key":"ref66","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1017\/S0007114514001238","article-title":"Reduced insulin clearance and lower insulin-degrading enzyme expression in the liver might contribute to the thrifty phenotype of protein-restricted mice","volume":"112","author":"LF Rezende","year":"2014","journal-title":"Br J Nutr"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.bbr.2015.11.031","article-title":"Methyl donor supplementation in rats reverses the deleterious effect of maternal separation on depression-like behaviour","volume":"299","author":"L Paternain","year":"2016","journal-title":"Behav Brain Res"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.cobeha.2015.12.004","article-title":"Stop signs in hippocampal insulin signaling: the role of insulin resistance in structural, functional and behavioral deficits","volume":"9","author":"JR Fadel","year":"2016","journal-title":"Curr Opin Behav Sci"},{"issue":"4","key":"ref69","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.1152\/physrev.00032.2015","article-title":"Brain Insulin Resistance at the Crossroads of Metabolic and Cognitive Disorders in Humans","volume":"96","author":"S Kullmann","year":"2016","journal-title":"Physiol Rev"},{"issue":"1","key":"ref70","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1023\/A:1022598900246","article-title":"Brain insulin: regulation, mechanisms of action and functions","volume":"23","author":"K Gerozissis","year":"2003","journal-title":"Cell Mol Neurobiol"},{"issue":"1","key":"ref71","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1002\/dev.10086","article-title":"Neonatal social isolation alters both maternal and pup behaviors in rats","volume":"42","author":"B Zimmerberg","year":"2003","journal-title":"Dev Psychobiol"},{"issue":"1","key":"ref72","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/npp.2015.171","article-title":"Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex","volume":"41","author":"BS McEwen","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"ref73","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.brainres.2014.10.051","article-title":"Maternal stress, nutrition and physical activity: Impact on immune function, CNS development and psychopathology","volume":"1617","author":"AH Marques","year":"2015","journal-title":"Brain Res"},{"key":"ref74","doi-asserted-by":"crossref","DOI":"10.3389\/fendo.2014.00161","article-title":"Insulin in the brain: its pathophysiological implications for States related with central insulin resistance, type 2 diabetes and Alzheimer\u2019s disease","volume":"5","author":"E Bl\u00e1zquez","year":"2014","journal-title":"Front Endocrinol"}],"updated-by":[{"DOI":"10.1371\/journal.pone.0210893","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2019,1,10]],"date-time":"2019-01-10T00:00:00Z","timestamp":1547078400000}}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0204731","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,11]],"date-time":"2024-07-11T13:35:15Z","timestamp":1720704915000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0204731"}},"subtitle":[],"editor":[{"given":"Alexandra","family":"Kavushansky","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,10,17]]},"references-count":74,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2018,10,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0204731","relation":{"correction":[{"id-type":"doi","id":"10.1371\/journal.pone.0210893","asserted-by":"object"}]},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,10,17]]}}}