{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T15:07:09Z","timestamp":1772118429109,"version":"3.50.1"},"reference-count":91,"publisher":"Wiley","issue":"6","license":[{"start":{"date-parts":[[2021,8,22]],"date-time":"2021-08-22T00:00:00Z","timestamp":1629590400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Developmental Psychobiology"],"published-print":{"date-parts":[[2021,9]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Data in both humans and preclinical animal models clearly indicate drug exposure during adolescence, when the \u201creward\u201d circuitry of the brain develops, increases the risk of substance use and other mental health disorders later in life. Human data indicate that different neural and behavioral sequelae can be observed in early versus late adolescence. However, most studies with rodent models examine a single adolescent age compared to a mature adult age, and often only in males. Herein, we sought to determine whether the acute response to the opioid morphine would also differ across adolescence, and by sex. By quantifying Fos positive cells, a proxy for neural activity, at different stages during adolescence (pre\u2010, early, mid\u2010, and late adolescence) and in multiple reward regions (prefrontal cortex, nucleus accumbens, caudate\/putamen), we determined that the neural response to acute morphine is highly dependent on adolescent age, sex, and brain region. These data suggest that heterogeneity in the consequences of adolescent opioid exposure may be due to age\u2010 and sex\u2010specific developmental profiles in individual reward processing regions. In future studies, it will be important to add age within adolescence as an independent variable for a holistic view of healthy or abnormal reward\u2010related neural development.<\/jats:p>","DOI":"10.1002\/dev.22186","type":"journal-article","created":{"date-parts":[[2021,8,23]],"date-time":"2021-08-23T01:50:20Z","timestamp":1629683420000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Morphine exposure alters Fos expression in a sex\u2010, age\u2010, and brain region\u2010specific manner during adolescence"],"prefix":"10.1002","volume":"63","author":[{"given":"C.","family":"Figueroa","sequence":"first","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"H.","family":"Yang","sequence":"additional","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"},{"name":"Northeastern University Boston MA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"DiSpirito","sequence":"additional","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"},{"name":"Rensselaer Polytechnic Institute Troy NY USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J. R.","family":"Bourgeois","sequence":"additional","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"G.","family":"Kalyanasundaram","sequence":"additional","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"I.","family":"Doshi","sequence":"additional","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S. D.","family":"Bilbo","sequence":"additional","affiliation":[{"name":"Deptartment of Psychology and Neuroscience Duke University Durham NC USA"},{"name":"Deptartment of Pediatrics Massachusetts General Hospital Boston MA USA"},{"name":"Lurie Center for Autism Harvard Medical School Boston MA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0195-8707","authenticated-orcid":false,"given":"A. M.","family":"Kopec","sequence":"additional","affiliation":[{"name":"Deptartment of Neuroscience &amp; Experimental Therapeutics Albany Medical College Albany NY USA"},{"name":"Deptartment of Pediatrics Massachusetts General Hospital Boston MA USA"},{"name":"Lurie Center for Autism Harvard Medical School Boston MA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2021,8,22]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0893-133X(02)00295-6"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1097\/ALN.0b013e318238bba6"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1097\/00001756-199704140-00034"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.1002\/1098-2396(200008)37:2<167::AID-SYN11>3.0.CO;2-B"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00213-013-3095-8"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41386-018-0127-4"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2013.02.063"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41386-018-0125-6"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(96)00541-6"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0304-3959(99)00246-8"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1002\/dev.22037"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.17-21-08596.1997"},{"key":"e_1_2_7_14_1","article-title":"A semi\u2010automated brain atlas\u2010based analysis pipeline for c\u2010Fos immunohistochemical data","author":"Bourgeois J. R.","year":"2020","journal-title":"Journal of Neuroscience Methods"},{"key":"e_1_2_7_15_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1471-4159.2000.0751625.x"},{"key":"e_1_2_7_16_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2003601117"},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1210\/en.2016-1160"},{"key":"e_1_2_7_18_1","doi-asserted-by":"publisher","DOI":"10.1152\/jn.00257.2018"},{"key":"e_1_2_7_19_1","doi-asserted-by":"publisher","DOI":"10.3389\/fendo.2018.00173"},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1196\/annals.1440.010"},{"key":"e_1_2_7_21_1","doi-asserted-by":"crossref","first-page":"403","DOI":"10.55782\/ane-2000-1359","article-title":"Molecular maps of neural activity and quiescence","volume":"60","author":"Chaudhuri A.","year":"2000","journal-title":"Acta Neurobiologiae Experimentalis (Wars)"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuropharm.2020.108243"},{"key":"e_1_2_7_23_1","first-page":"14","article-title":"Age\u2010related differences in the sensitivity of serum luteinizing hormone to prototypic mu, kappa and delta opiate agonists and antagonists","volume":"246","author":"Cicero T. J.","year":"1988","journal-title":"Journal of Pharmacology and Experimental Therapeutics"},{"key":"e_1_2_7_24_1","first-page":"627","article-title":"Ontogeny of the opioid\u2010mediated control of reproductive endocrinology in the male and female rat","volume":"236","author":"Cicero T. J.","year":"1986","journal-title":"Journal of Pharmacology and Experimental Therapeutics"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.genm.2010.09.004"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejpain.2007.07.014"},{"key":"e_1_2_7_27_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(85)90489-5"},{"key":"e_1_2_7_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbb.2006.12.001"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1097\/FBP.0000000000000622"},{"key":"e_1_2_7_30_1","doi-asserted-by":"publisher","DOI":"10.1002\/jnr.23878"},{"key":"e_1_2_7_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(99)00229-8"},{"key":"e_1_2_7_32_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.2906-16.2017"},{"key":"e_1_2_7_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.physbeh.2017.11.030"},{"key":"e_1_2_7_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbb.2012.12.009"},{"key":"e_1_2_7_35_1","doi-asserted-by":"publisher","DOI":"10.1038\/sj.npp.1300465"},{"key":"e_1_2_7_36_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-psych-010213-115159"},{"key":"e_1_2_7_37_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00787-017-1068-x"},{"key":"e_1_2_7_38_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-8993(99)01709-6"},{"key":"e_1_2_7_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(02)00975-2"},{"key":"e_1_2_7_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(95)00625-Z"},{"key":"e_1_2_7_41_1","doi-asserted-by":"publisher","DOI":"10.1139\/y98-027"},{"key":"e_1_2_7_42_1","first-page":"192","article-title":"Differential effects of antipsychotic and psychotomimetic drugs on neurotensin systems of discrete extrapyramidal and limbic regions","volume":"270","author":"Gygi S. P.","year":"1994","journal-title":"Journal of Pharmacology and Experimental Therapeutics"},{"key":"e_1_2_7_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbr.2015.04.008"},{"key":"e_1_2_7_44_1","doi-asserted-by":"publisher","DOI":"10.1542\/peds.2017-2439"},{"key":"e_1_2_7_45_1","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2018.9023"},{"key":"e_1_2_7_46_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.neuro.31.060407.125533"},{"key":"e_1_2_7_47_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.12-02-00483.1992"},{"key":"e_1_2_7_48_1","doi-asserted-by":"publisher","DOI":"10.1111\/nyas.13961"},{"key":"e_1_2_7_49_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-06118-z"},{"key":"e_1_2_7_50_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.addbeh.2015.06.024"},{"key":"e_1_2_7_51_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.91.18.8537"},{"key":"e_1_2_7_52_1","doi-asserted-by":"publisher","DOI":"10.1002\/dev.20468"},{"key":"e_1_2_7_53_1","doi-asserted-by":"publisher","DOI":"10.1677\/joe.0.1290253"},{"key":"e_1_2_7_54_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2014.04.030"},{"key":"e_1_2_7_55_1","doi-asserted-by":"publisher","DOI":"10.1101\/lm.022889.111"},{"key":"e_1_2_7_56_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.drugalcdep.2018.10.027"},{"key":"e_1_2_7_57_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1360-0443.2007.02015.x"},{"key":"e_1_2_7_58_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41386-018-0138-1"},{"key":"e_1_2_7_59_1","doi-asserted-by":"publisher","DOI":"10.1542\/peds.2015-1364"},{"key":"e_1_2_7_60_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.1366-03.2004"},{"key":"e_1_2_7_61_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2014.12.024"},{"key":"e_1_2_7_62_1","doi-asserted-by":"publisher","DOI":"10.1002\/dev.21137"},{"key":"e_1_2_7_63_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.3037702"},{"key":"e_1_2_7_64_1","doi-asserted-by":"publisher","DOI":"10.1038\/38730"},{"key":"e_1_2_7_65_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tics.2004.12.008"},{"key":"e_1_2_7_66_1","volume-title":"The rat brain in stereotactic coordinates","author":"Paxinos G.","year":"2006"},{"key":"e_1_2_7_67_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00213-011-2335-z"},{"key":"e_1_2_7_68_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuropharm.2017.01.036"},{"key":"e_1_2_7_69_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2010.03.036"},{"key":"e_1_2_7_70_1","unstructured":"SAMSHA SAaMHSA. (2020).Key substance use and mental health indicators in the United States: Results from the 2019 National Survey on Drug use and Health. (HHS Publication No. PEP20\u201007\u201001\u2010001 NSDUH Series H\u201055).Rockville MD:Center for Behavioral Health Statistics and Quality Substance Abuse and Mental Health Services Administration."},{"key":"e_1_2_7_71_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00441-013-1581-2"},{"key":"e_1_2_7_72_1","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.2516-12.2013"},{"key":"e_1_2_7_73_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejphar.2004.01.012"},{"key":"e_1_2_7_74_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainresbull.2003.08.002"},{"key":"e_1_2_7_75_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00429-017-1498-8"},{"key":"e_1_2_7_76_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2015.05.019"},{"key":"e_1_2_7_77_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0149-7634(00)00014-2"},{"key":"e_1_2_7_78_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.physbeh.2015.01.027"},{"key":"e_1_2_7_79_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2016.07.026"},{"key":"e_1_2_7_80_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0736-5748(99)00108-2"},{"key":"e_1_2_7_81_1","doi-asserted-by":"publisher","DOI":"10.1159\/000017365"},{"key":"e_1_2_7_82_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2009.06.001"},{"key":"e_1_2_7_83_1","first-page":"1028","article-title":"Forebrain sites differentially sensitive to beta\u2010endorphin and morphine for analgesia and release of Met\u2010enkephalin in the pentobarbital\u2010anesthesized rat","volume":"261","author":"Tseng L. F.","year":"1992","journal-title":"Journal of Pharmacology and Experimental Therapeutics"},{"key":"e_1_2_7_84_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41386-018-0225-3"},{"key":"e_1_2_7_85_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neubiorev.2016.07.025"},{"key":"e_1_2_7_86_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2019.02.006"},{"key":"e_1_2_7_87_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.alcohol.2014.01.012"},{"key":"e_1_2_7_88_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1200130109"},{"key":"e_1_2_7_89_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00429-011-0353-6"},{"key":"e_1_2_7_90_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1460-9568.2012.08101.x"},{"key":"e_1_2_7_91_1","doi-asserted-by":"publisher","DOI":"10.1113\/JP270492"},{"key":"e_1_2_7_92_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(99)00309-7"}],"container-title":["Developmental Psychobiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/dev.22186","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/dev.22186","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/dev.22186","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,6]],"date-time":"2024-09-06T22:18:28Z","timestamp":1725661108000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/dev.22186"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,22]]},"references-count":91,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2021,9]]}},"alternative-id":["10.1002\/dev.22186"],"URL":"https:\/\/doi.org\/10.1002\/dev.22186","archive":["Portico"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.04.29.441958","asserted-by":"object"}]},"ISSN":["0012-1630","1098-2302"],"issn-type":[{"value":"0012-1630","type":"print"},{"value":"1098-2302","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,22]]},"assertion":[{"value":"2021-04-29","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2021-08-08","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2021-08-22","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e22186"}}