{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T02:52:47Z","timestamp":1791168767006,"version":"4.1.0"},"reference-count":54,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2014,4,1]],"date-time":"2014-04-01T00:00:00Z","timestamp":1396310400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"}],"funder":[{"DOI":"10.13039\/501100003074","name":"Agencia Nacional de Promoci\u00f3n Cient\u00edfica y Tecnol\u00f3gica","doi-asserted-by":"publisher","award":["PICT2011-0196"],"award-info":[{"award-number":["PICT2011-0196"]}],"id":[{"id":"10.13039\/501100003074","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005363","name":"Universidad de Buenos Aires","doi-asserted-by":"crossref","award":["UBACyT2011-284"],"award-info":[{"award-number":["UBACyT2011-284"]}],"id":[{"id":"10.13039\/501100005363","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100008056","name":"Fundaci\u00f3n Florencio Fiorini","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100008056","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Physiology &amp; Behavior"],"published-print":{"date-parts":[[2014,4]]},"DOI":"10.1016\/j.physbeh.2014.02.051","type":"journal-article","created":{"date-parts":[[2014,3,7]],"date-time":"2014-03-07T14:16:12Z","timestamp":1394201772000},"page":"237-254","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":89,"special_numbering":"C","title":["Early protein malnutrition negatively impacts physical growth and neurological reflexes and evokes anxiety and depressive-like behaviors"],"prefix":"10.1016","volume":"129","author":[{"given":"Laura M.","family":"Belluscio","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruno G.","family":"Berardino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadina M.","family":"Ferroni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julieta M.","family":"Ceruti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4322-1650","authenticated-orcid":false,"given":"Eduardo T.","family":"C\u00e1nepa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.physbeh.2014.02.051_bb0005","series-title":"The state of food insecurity in the world","author":"FAO","year":"2012"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0010","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.2014.02.051_bb0015","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/S0140-6736(13)60937-X","article-title":"Maternal and child undernutrition and overweight in low-income and middle-income countries","volume":"382","author":"Black","year":"2013","journal-title":"Lancet"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0020","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1016\/j.neubiorev.2012.03.009","article-title":"Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat","volume":"36","author":"Alamy","year":"2012","journal-title":"Neurosci Biobehav Rev"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0025","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1016\/j.cell.2004.11.040","article-title":"Accelerated evolution of nervous system genes in the origin of Homo sapiens","volume":"119","author":"Dorus","year":"2004","journal-title":"Cell"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0030","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1079\/PHN2005805","article-title":"Review of the evidence linking protein and energy to mental development","volume":"8","author":"Grantham-McGregor","year":"2005","journal-title":"Public Health Nutr"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0035","doi-asserted-by":"crossref","first-page":"2167","DOI":"10.1113\/jphysiol.2011.223305","article-title":"Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function","volume":"590","author":"Connor","year":"2013","journal-title":"J Physiol"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0040","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/S0149-7634(02)00012-X","article-title":"Effects of prenatal protein malnutrition on the hippocampal formation","volume":"26","author":"Morgane","year":"2002","journal-title":"Neurosci Biobehav Rev"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0045","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1038\/mp.2011.107","article-title":"Epigenetic regulation of the BDNF gene: implications for psychiatric disorders","volume":"17","author":"Boulle","year":"2012","journal-title":"Mol Psychiatry"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0050","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.brainres.2007.02.031","article-title":"Stress-induced changes in extracellular dopamine and serotonin in the medial prefrontal cortex and dorsal hippocampus of prenatally malnourished rats","volume":"1148","author":"Mokler","year":"2007","journal-title":"Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0055","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.neulet.2006.07.052","article-title":"Effects of maternal protein malnutrition on oxidative markers in the young rat cortex and cerebellum","volume":"406","author":"Bonatto","year":"2006","journal-title":"Neurosci Lett"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0060","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/S0165-3806(97)00109-0","article-title":"Maternal protein restriction early in rat pregnancy alters brain development in the progeny","volume":"103","author":"Gressens","year":"1997","journal-title":"Brain Res Dev Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0065","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1023\/A:1024272227219","article-title":"Effects of undernutrition on glutamatergic parameters in rat brain","volume":"28","author":"Rotta","year":"2003","journal-title":"Neurochem Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0070","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.brainres.2012.10.047","article-title":"Effects of protein restriction during gestation and lactation on cell proliferation in the hippocampus and subventricular zone: functional implications. Protein restriction alters hippocampal\/SVZ cell proliferation","volume":"1496","author":"Godoy","year":"2013","journal-title":"Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0075","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.2014.02.051_bb0080","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.2014.02.051_bb0085","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.bbr.2011.06.008","article-title":"Pre- and\/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats","volume":"227","author":"Reyes-Castro","year":"2012","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0090","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1179\/147683010X12611460764769","article-title":"Effects of postnatal protein malnutrition on learning and memory procedures","volume":"13","author":"Valadares","year":"2010","journal-title":"Nutr Neurosci"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0095","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1016\/S0031-9384(96)80047-3","article-title":"Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test","volume":"60","author":"Almeida","year":"1996","journal-title":"Physiol Behav"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0100","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.2014.02.051_bb0105","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/S0736-5748(96)00121-9","article-title":"Postnatal changes of brain monoamine levels in prenatally malnourished and control rats","volume":"15","author":"Chen","year":"1997","journal-title":"Int J Dev Neurosci"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0110","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/0091-3057(94)90439-1","article-title":"Effects of early protein malnutrition and environmental stimulation upon the reactivity to diazepam in two animal models of anxiety","volume":"49","author":"Santucci","year":"1994","journal-title":"Pharmacol Biochem Behav"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0115","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brainresbull.2010.06.005","article-title":"Effects of maternal food restriction on physical growth and neurobehavior in newborn Wistar rats","volume":"83","author":"Zhang","year":"2010","journal-title":"Brain Res Bull"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0120","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.1056\/NEJM199904223401603","article-title":"Birth weight in relation to morbidity and mortality among newborn infants","volume":"340","author":"McIntire","year":"1999","journal-title":"N Engl J Med"},{"issue":"Suppl. 3","key":"10.1016\/j.physbeh.2014.02.051_bb0125","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.2014.02.051_bb0130","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1186\/1744-9081-4-31","article-title":"Cognitive development in children with chronic protein energy malnutrition","volume":"4","author":"Kar","year":"2008","journal-title":"Behav Brain Funct"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0135","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1016\/j.neuro.2007.01.014","article-title":"Extrapolating brain development from experimental species to humans","volume":"28","author":"Clancy","year":"2007","journal-title":"Neurotoxicology"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0140","doi-asserted-by":"crossref","first-page":"7368","DOI":"10.1523\/JNEUROSCI.5746-12.2013","article-title":"Modeling transformations of neurodevelopmental sequences across mammalian species","volume":"33","author":"Workman","year":"2013","journal-title":"J Neurosci"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0145","first-page":"13","article-title":"Neurobiology of posttraumatic stress disorder","volume":"14","author":"Heim","year":"2009","journal-title":"CNS Spectr"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0150","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1016\/j.bbr.2011.07.037","article-title":"Early-life stress mediated modulation of adult neurogenesis and behavior","volume":"227","author":"Korosi","year":"2012","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0155","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1097\/YCO.0b013e3283477ad5","article-title":"Sex differences in the disability associated with mental disorders","volume":"24","author":"Scott","year":"2011","journal-title":"Curr Opin Psychiatry"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0160","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.1093\/jn\/123.11.1939","article-title":"AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet","volume":"123","author":"Reeves","year":"1993","journal-title":"J Nutr"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0165","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1111\/j.1601-183X.2007.00330.x","article-title":"Autism-like behavioral phenotypes in BTBR T+tf\/J mice","volume":"7","author":"McFarlane","year":"2008","journal-title":"Genes Brain Behav"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0170","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1111\/j.1601-183X.2011.00688.x","article-title":"Sex differences in juvenile mouse social behavior are influenced by sex chromosomes and social context","volume":"10","author":"Cox","year":"2011","journal-title":"Genes Brain Behav"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0175","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/00401706.1969.10490657","article-title":"Procedures for detecting outlying observations in samples","volume":"11","author":"Grubbs","year":"1969","journal-title":"Technometrics"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0180","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1093\/jn\/118.7.883","article-title":"Effect of chronic protein-energy malnutrition on fecundability, fecundity and fertility in rats","volume":"118","author":"Alexander","year":"1988","journal-title":"J Nutr"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0185","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/1471-213X-8-52","article-title":"The transcription factor Nfix is essential for normal brain development","volume":"8","author":"Campbell","year":"2008","journal-title":"BMC Dev Biol"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0190","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.1016\/j.neuroscience.2006.04.059","article-title":"A neural cell adhesion molecule-derived fibroblast growth factor receptor agonist, the FGL-peptide, promotes early postnatal sensorimotor development and enhances social memory retention","volume":"141","author":"Secher","year":"2006","journal-title":"Neuroscience"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0195","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1124\/mol.59.3.442","article-title":"Molecular targets for the myorelaxant action of diazepam","volume":"59","author":"Crestani","year":"2001","journal-title":"Mol Pharmacol"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0200","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1038\/nn1276","article-title":"Epigenetic programming by maternal behavior","volume":"7","author":"Weaver","year":"2004","journal-title":"Nat Neurosci"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0205","doi-asserted-by":"crossref","first-page":"5335","DOI":"10.1073\/pnas.95.9.5335","article-title":"Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat","volume":"95","author":"Caldji","year":"1998","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0210","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1126\/science.286.5442.1155","article-title":"Nongenomic transmission across generations of maternal behavior and stress responses in the rat","volume":"286","author":"Francis","year":"1999","journal-title":"Science"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0215","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.psyneuen.2006.12.012","article-title":"Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring: implications for postpartum mood disorder","volume":"32","author":"Bosch","year":"2007","journal-title":"Psychoneuroendocrinology"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0220","doi-asserted-by":"crossref","first-page":"e2210","DOI":"10.1371\/journal.pone.0002210","article-title":"Maternal programming of sexual behavior and hypothalamic\u2013pituitary\u2013gonadal function in the female rat","volume":"3","author":"Cameron","year":"2008","journal-title":"PLoS One"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0225","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.2014.02.051_bb0230","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1002\/(SICI)1098-2302(199903)34:2<129::AID-DEV6>3.0.CO;2-L","article-title":"Play is indispensable for an adequate development of coping with social challenges in the rat","volume":"34","author":"van den Berg","year":"1999","journal-title":"Dev Psychobiol"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0235","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1007\/s002130100694","article-title":"Sensitivity to the effects of pharmacologically selective antidepressants in different strains of mice","volume":"155","author":"Lucki","year":"2001","journal-title":"Psychopharmacology (Berl)"},{"issue":"Suppl. 14","key":"10.1016\/j.physbeh.2014.02.051_bb0240","first-page":"22","article-title":"Anxiety associated with comorbid depression","volume":"63","author":"Moller","year":"2002","journal-title":"J Clin Psychiatry"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0245","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.devbrainres.2004.10.013","article-title":"Gestational and postnatal malnutrition affects sensitivity of young rats to picrotoxin and quinolinic acid and uptake of GABA by cortical and hippocampal slices","volume":"154","author":"Schweigert","year":"2005","journal-title":"Brain Res Dev Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0250","first-page":"E270","article-title":"Protein restriction during pregnancy affects maternal liver lipid metabolism and fetal brain lipid composition in the rat","volume":"298","author":"Torres","year":"2009","journal-title":"Am J Physiol"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0255","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.bbr.2009.05.031","article-title":"Effect of early malnutrition and environmental stimulation in the performance of rats in the elevated plus maze","volume":"205","author":"Pereira-da-Silva","year":"2009","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0260","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":"da Silva","year":"2005","journal-title":"Behav Brain Res"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0265","doi-asserted-by":"crossref","first-page":"2369","DOI":"10.1093\/hmg\/ddi239","article-title":"Profound ataxia in complexin I knockout mice masks a complex phenotype that includes exploratory and habituation deficits","volume":"14","author":"Glynn","year":"2005","journal-title":"Hum Mol Genet"},{"key":"10.1016\/j.physbeh.2014.02.051_bb0270","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1212\/WNL.43.3_Part_1.505","article-title":"Dopamine-related personality traits in Parkinson's disease","volume":"43","author":"Menza","year":"1993","journal-title":"Neurology"}],"container-title":["Physiology &amp; Behavior"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938414001218?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0031938414001218?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2019,8,8]],"date-time":"2019-08-08T03:26:13Z","timestamp":1565234773000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0031938414001218"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,4]]},"references-count":54,"alternative-id":["S0031938414001218"],"URL":"https:\/\/doi.org\/10.1016\/j.physbeh.2014.02.051","relation":{},"ISSN":["0031-9384"],"issn-type":[{"value":"0031-9384","type":"print"}],"subject":[],"published":{"date-parts":[[2014,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Early protein malnutrition negatively impacts physical growth and neurological reflexes and evokes anxiety and depressive-like behaviors","name":"articletitle","label":"Article Title"},{"value":"Physiology & Behavior","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.physbeh.2014.02.051","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2014 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}