{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T10:21:09Z","timestamp":1778581269849,"version":"3.51.4"},"reference-count":46,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2018,10,9]],"date-time":"2018-10-09T00:00:00Z","timestamp":1539043200000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000104","name":"National Aeronautics and Space Administration","doi-asserted-by":"publisher","award":["NNX12AB54G"],"award-info":[{"award-number":["NNX12AB54G"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Genet."],"DOI":"10.3389\/fgene.2018.00404","type":"journal-article","created":{"date-parts":[[2018,10,9]],"date-time":"2018-10-09T15:11:35Z","timestamp":1539097895000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["Space Radiation Alters Genotype\u2013Phenotype Correlations in Fear Learning and Memory Tests"],"prefix":"10.3389","volume":"9","author":[{"given":"Ovidiu Dan","family":"Iancu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sydney Weber","family":"Boutros","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Reid H. J.","family":"Olsen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Matthew J.","family":"Davis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Blair","family":"Stewart","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Massarra","family":"Eiwaz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tessa","family":"Marzulla","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John","family":"Belknap","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christina M.","family":"Fallgren","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elijah F.","family":"Edmondson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael M.","family":"Weil","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacob","family":"Raber","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2018,10,9]]},"reference":[{"key":"B1","author":"Alfaia","year":"2007","journal-title":"Gamma Irradiation Effect on Fatty Acid Composition and Conjugated Linoleic Acid Isomers of Lamb Meat."},{"key":"B2","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1002\/1098-1063(2001)11:1<8::AID-HIPO1015>3.0.CO;2-7","article-title":"Hippocampus and contextual fear conditioning: recent controversies and advances.","volume":"11","author":"Anagnostaras","year":"2001","journal-title":"Hippocampus"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2010.00158","article-title":"Automated assessment of pavlovian conditioned freezing and shock reactivity in mice using the video freeze system.","volume":"4","author":"Anagnostaras","year":"2010","journal-title":"Front. Behav. Neurosci."},{"key":"B4","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1186\/1479-7364-2-6-345","article-title":"Testing groups of genomic locations for enrichment in disease loci using linkage scan data: a method for hypothesis testing.","volume":"2","author":"Avramopoulos","year":"2006","journal-title":"Hum. Genomics"},{"key":"B5","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1242\/dmm.027789","article-title":"Identifying genes for neurobehavioural traits in rodents: progress and pitfalls.","volume":"10","author":"Baud","year":"2017","journal-title":"Dis. Model. Mech."},{"key":"B6","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1016\/j.ynstr.2014.10.004","article-title":"Stress, social behavior, and resilience: insights from rodents.","volume":"1","author":"Beery","year":"2015","journal-title":"Neurobiol. Stress"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-1068","article-title":"Limits on the reproducibility of marker associations with southern leaf blight resistance in the maize nested association mapping population.","volume":"15","author":"Bian","year":"2014","journal-title":"BMC Genomics"},{"key":"B8","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1111\/j.1467-8721.2009.01622.x","article-title":"Genes in Context: gene\u2013environment interplay and the origins of individual differences in behavior.","volume":"18","author":"Champagne","year":"2009","journal-title":"Curr. Dir. Psychol. Sci."},{"key":"B9","first-page":"169","article-title":"Effects of total body irradiation on fatty acid and total lipid content of rats.","volume":"25","author":"Chukwuemeka","year":"2012","journal-title":"Pak. J. Pharm. Sci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/s002130050327","article-title":"Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies.","volume":"132","author":"Crawley","year":"1997","journal-title":"Psychopharmacology"},{"key":"B11","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1093\/genetics\/131.2.479","article-title":"Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data.","volume":"131","author":"Excoffier","year":"1992","journal-title":"Genetics"},{"key":"B12","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1002\/neu.10161","article-title":"Analysis of quantitative trait loci that influence animal behavior.","volume":"54","author":"Flint","year":"2003","journal-title":"J. Neurobiol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"594","DOI":"10.1111\/j.1749-6632.1968.tb11919.x","article-title":"The effect of irradiation on plasma esterases in mice.","volume":"151","author":"Hunter","year":"1968","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"B14","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1016\/j.neuron.2010.12.034","article-title":"Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans.","volume":"69","author":"Indovina","year":"2011","journal-title":"Neuron"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1177\/1010428317749676","article-title":"Anticancer redox activity of gallium nanoparticles accompanied with low dose of gamma radiation in female mice.","volume":"40","author":"Kandil","year":"2018","journal-title":"Tumour Biol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"13744","DOI":"10.1073\/pnas.1704907114","article-title":"Machine learning shows association between genetic variability in PPARG and cerebral connectivity in preterm infants.","volume":"114","author":"Krishnan","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.bbr.2015.10.050","article-title":"Post-training gamma irradiation-enhanced contextual fear memory associated with reduced neuronal activation of the infralimbic cortex.","volume":"298","author":"Kugelman","year":"2016","journal-title":"Behav. Brain Res."},{"key":"B18","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1258\/0023677041958945","article-title":"Experimental animal urine collection: a review.","volume":"38","author":"Kurien","year":"2004","journal-title":"Lab. Anim."},{"key":"B19","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1038\/ijo.2012.82","article-title":"Challenges in reproducibility of genetic association studies: lessons learned from the obesity field.","volume":"37","author":"Li","year":"2013","journal-title":"Int. J. Obes."},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.3389\/fnana.2015.00120","article-title":"PPAR\u03b3 mRNA in the adult mouse hypothalamus: distribution and regulation in response to dietary challenges.","volume":"9","author":"Liu","year":"2015","journal-title":"Front. Neuroanat."},{"key":"B21","first-page":"209","article-title":"The detection of disease clustering and a generalized regression approach.","volume":"27","author":"Mantel","year":"1967","journal-title":"Cancer Res."},{"key":"B22","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1007\/978-1-60761-883-6_5","article-title":"\u201cFear conditioning in rodents and humans,\u201d in","author":"Milad","year":"2011","journal-title":"Animal Models of Behavioral Analysis Neuromethods"},{"key":"B23","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1667\/RR13828.1","article-title":"Energy metabolism in a matched model of radiation resistance for head and neck squamous cell cancer.","volume":"183","author":"Mims","year":"2015","journal-title":"Radiat. Res."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2014.00231","article-title":"Impairment in extinction of contextual and cued fear following post-training whole-body irradiation.","volume":"8","author":"Olsen","year":"2014","journal-title":"Front. Behav. Neurosci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1016\/S0306-4522(97)00165-6","article-title":"Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses.","volume":"80","author":"Owen","year":"1997","journal-title":"Neuroscience"},{"key":"B26","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1037\/0735-7044.108.4.810","article-title":"DBA\/2 and C57BL\/6 mice differ in contextual fear but not auditory fear conditioning.","volume":"108","author":"Paylor","year":"1994","journal-title":"Behav. Neurosci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1080\/09553009414551581","article-title":"Effect of radiation quality on lesion complexity in cellular DNA.","volume":"66","author":"Prise","year":"1994","journal-title":"Int. J. Radiat. Biol."},{"key":"B28","year":"2018","journal-title":"R: A Language and Environment for Statistical Computing."},{"key":"B29","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.bbr.2013.02.022","article-title":"Effects of whole body (56) Fe radiation on contextual freezing and Arc-positive cells in the dentate gyrus.","volume":"246","author":"Raber","year":"2013","journal-title":"Behav. Brain Res."},{"key":"B30","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.lssr.2015.10.004","article-title":"(16)Oxygen irradiation enhances cued fear memory in B6D2F1 mice.","volume":"7","author":"Raber","year":"","journal-title":"Life Sci. Space Res."},{"key":"B31","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1667\/RR13951.1","article-title":"28Silicon irradiation impairs contextual fear memory in B6D2F1 mice.","volume":"183","author":"Raber","year":"","journal-title":"Radiat. Res."},{"key":"B32","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1667\/RR13347.1","article-title":"(28)Silicon radiation-induced enhancement of synaptic plasticity in the hippocampus of na\u00efve and cognitively tested mice.","volume":"181","author":"Raber","year":"2014","journal-title":"Radiat. Res."},{"key":"B33","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.lssr.2016.03.002","article-title":"Sex- and dose-dependent effects of calcium ion irradiation on behavioral performance of B6D2F1 mice during contextual fear conditioning training.","volume":"9","author":"Raber","year":"2016","journal-title":"Life Sci. Space Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"482","DOI":"10.1667\/RR14173.1","article-title":"Inhibition of fatty acid synthase sensitizes prostate cancer cells to radiotherapy.","volume":"184","author":"Rae","year":"2015","journal-title":"Radiat. Res."},{"key":"B35","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1007\/s00335-007-9045-1","article-title":"The polymorphism architecture of mouse genetic resources elucidated using genome-wide resequencing data: implications for QTL discovery and systems genetics.","volume":"18","author":"Roberts","year":"2007","journal-title":"Mamm. Genome"},{"key":"B36","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1016\/S0022-2275(20)37707-5","article-title":"Radiation inactivation analysis of acyl-CoA: retinol acyltransferase and lecithin: retinol acyltransferase in rat liver.","volume":"34","author":"Ross","year":"1993","journal-title":"J. Lipid Res."},{"key":"B37","doi-asserted-by":"publisher","first-page":"17501","DOI":"10.1073\/pnas.0607207103","article-title":"Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus.","volume":"103","author":"Saxe","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1111\/1755-0998.12780","article-title":"Success and failure in replication of genotype-phenotype associations: how does replication help in understanding the genetic basis of phenotypic variation in outbred populations?","author":"Schielzeth","year":"2018","journal-title":"Mol. Ecol. Resour."},{"key":"B39","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1002\/gepi.1115","article-title":"Mantel statistics to correlate gene expression levels from microarrays with clinical covariates.","volume":"23","author":"Shannon","year":"2002","journal-title":"Genet. Epidemiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1359\/JBMR.041129","article-title":"Nonreplication in genetic studies of complex diseases\u2013lessons learned from studies of osteoporosis and tentative remedies.","volume":"20","author":"Shen","year":"2005","journal-title":"J. Bone Miner. Res."},{"key":"B41","author":"Stuster","year":"2016","journal-title":"Behavioral Issues Associated with Long-Duration Space Expeditions: Review and Analysis of Astronaut Journals Experiment 01-E104 (Journals) Phase 2 Final Report."},{"key":"B42","doi-asserted-by":"publisher","first-page":"879","DOI":"10.1038\/ng1840","article-title":"Genome-wide genetic association of complex traits in heterogeneous stock mice.","volume":"38","author":"Valdar","year":"2006","journal-title":"Nat. Genet."},{"key":"B43","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1002\/hipo.20659","article-title":"Sex-dependent effects of 56Fe irradiation on contextual fear conditioning in C57BL\/6J mice.","volume":"20","author":"Villasana","year":"2010","journal-title":"Hippocampus"},{"key":"B44","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1667\/RR3107","article-title":"Retinoids and TIMP1 prevent radiation-induced apoptosis of capillary endothelial cells.","volume":"161","author":"Vorotnikova","year":"2004","journal-title":"Radiat. Res."},{"key":"B45","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1038\/ng1197-331","article-title":"Quantitative trait locus analysis of contextual fear conditioning in mice.","volume":"17","author":"Wehner","year":"1997","journal-title":"Nat. Genet."},{"key":"B46","doi-asserted-by":"publisher","first-page":"792","DOI":"10.1086\/508346","article-title":"Generalized genomic distance\u2013based regression methodology for multilocus association analysis.","volume":"79","author":"Wessel","year":"2006","journal-title":"Am. J. Hum. Genet."}],"container-title":["Frontiers in Genetics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fgene.2018.00404\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,3]],"date-time":"2022-09-03T17:29:52Z","timestamp":1662226192000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fgene.2018.00404\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,10,9]]},"references-count":46,"alternative-id":["10.3389\/fgene.2018.00404"],"URL":"https:\/\/doi.org\/10.3389\/fgene.2018.00404","relation":{},"ISSN":["1664-8021"],"issn-type":[{"value":"1664-8021","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,10,9]]},"article-number":"404"}}