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Paternal morphine self-administration produces object recognition memory deficits in female, but not male offspring

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Abstract

Rationale

Parental drug use around or before conception can have adverse consequences for offspring. Historically, this research has focused on the effects of maternal substance use on future generations but less is known about the influence of the paternal lineage. This study focused on the impact of chronic paternal morphine exposure prior to conception on behavioral outcomes in male and female progeny.

Objectives

This study sought to investigate the impact of paternal morphine self-administration on anxiety-like behavior, the stress response, and memory in male and female offspring.

Methods

Adult, drug-naïve male and female progeny of morphine-treated sires and controls were evaluated for anxiety-like behavior using defensive probe burying and novelty-induced hypophagia paradigms. Hypothalamic-pituitary-adrenal (HPA) axis function was assessed by measuring plasma corticosterone levels following a restraint stressor in male and female progeny. Memory was probed using a battery of tests including object location memory, novel object recognition, and contextual fear conditioning.

Results

Paternal morphine exposure did not alter anxiety-like behavior or stress-induced HPA axis activation in male or female offspring. Morphine-sired male and female offspring showed intact hippocampus-dependent memory: they performed normally on the long-term fear conditioning and object location memory tests. In contrast, paternal morphine exposure selectively disrupted novel object recognition in female, but not male, progeny.

Conclusions

Our findings demonstrate that paternal morphine taking produces sex-specific and selective impairments in object recognition memory while leaving hippocampal function largely intact.

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Abbreviations

HPA axis:

Hypothalamic-pituitary-adrenal axis

i.p.:

Intraperitoneal

FR:

Fixed ratio

PND:

Post-natal day

NIH:

Novelty-induced hypophagia

n.s.:

Non-significant

F1:

First generation (offspring)

References

  • Ahmadalipour A, Ghodrati-Jaldbakhan S, Samaei SA, Rashidy-Pour A (2018) Deleterious effects of prenatal exposure to morphine on the spatial learning and hippocampal BDNF and long-term potentiation in juvenile rats: beneficial influences of postnatal treadmill exercise and enriched environment. Neurobiol Learn Mem 147:54–64

    Article  CAS  PubMed  Google Scholar 

  • Akbarabadi A, Niknamfar S, Vousooghi N, Sadat-Shirazi MS, Toolee H, Zarrindast MR (2018) Effect of rat parental morphine exposure on passive avoidance memory and morphine conditioned place preference in male offspring. Physiol Behav 184:143–149

    Article  CAS  PubMed  Google Scholar 

  • Baldacchino A, Balfour DJ, Passetti F, Humphris G, Matthews K (2012) Neuropsychological consequences of chronic opioid use: a quantitative review and meta-analysis. Neurosci Biobehav Rev 36:2056–2068

    Article  CAS  PubMed  Google Scholar 

  • Bale TL (2015) Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci 16:332–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bali A, Randhawa PK, Jaggi AS (2015) Stress and opioids: role of opioids in modulating stress-related behavior and effect of stress on morphine conditioned place preference. Neurosci Biobehav Rev 51:138–150

    Article  CAS  PubMed  Google Scholar 

  • Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31:10721–10731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Block C, Cianfrini L (2013) Neuropsychological and neuroanatomical sequelae of chronic non-malignant pain and opioid analgesia. NeuroRehabilitation 33:343–366

    Article  PubMed  Google Scholar 

  • Byrnes EM (2005) Transgenerational consequences of adolescent morphine exposure in female rats: effects on anxiety-like behaviors and morphine sensitization in adult offspring. Psychopharmacology 182:537–544

    Article  CAS  PubMed  Google Scholar 

  • Byrnes JJ, Babb JA, Scanlan VF, Byrnes EM (2011) Adolescent opioid exposure in female rats: transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav Brain Res 218:200–205

    Article  CAS  PubMed  Google Scholar 

  • Byrnes JJ, Johnson NL, Carini LM, Byrnes EM (2013) Multigenerational effects of adolescent morphine exposure on dopamine D2 receptor function. Psychopharmacology 227:263–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calhoun S, Conner E, Miller M, Messina N (2015) Improving the outcomes of children affected by parental substance abuse: a review of randomized controlled trials. Subst Abus Rehabil 6:15–24

    Google Scholar 

  • Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD, Meissner A, Weng Z, Hofmann HA, Friedman N, Rando OJ (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castellano C (1980) Dose-dependent effects of heroin on memory in two inbred strains of mice. Psychopharmacology 67:235–239

    Article  CAS  PubMed  Google Scholar 

  • Chorbov VM, Todorov AA, Lynskey MT, Cicero TJ (2011) Elevated levels of DNA methylation at the OPRM1 promoter in blood and sperm from male opioid addicts. J Opioid Manag 7:258–264

    Article  PubMed  PubMed Central  Google Scholar 

  • Cicero TJ, Nock B, O’Connor L, Adams M, Meyer ER (1995) Adverse effects of paternal opiate exposure on offspring development and sensitivity to morphine-induced analgesia. J Pharmacol Exp Ther 273:386–392

    CAS  PubMed  Google Scholar 

  • Cicero TJ, Davis LA, LaRegina MC, Meyer ER, Schlegel MS (2002) Chronic opiate exposure in the male rat adversely affects fertility. Pharmacol Biochem Behav 72:157–163

    Article  CAS  PubMed  Google Scholar 

  • Degenhardt L, Whiteford H, Hall WD (2014) The Global Burden of Disease projects: what have we learned about illicit drug use and dependence and their contribution to the global burden of disease? Drug Alcohol Rev 33:4–12

    Article  PubMed  Google Scholar 

  • Donny EC, Bigelow GE, Walsh SL (2006) Comparing the physiological and subjective effects of self-administered vs yoked cocaine in humans. Psychopharmacology 186:544–552

    Article  CAS  PubMed  Google Scholar 

  • Dunn GA, Bale TL (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan L, Zhao Z, Orr PT, Chambers CH, Lewis MC, Frick KM (2010) Estradiol-induced object memory consolidation in middle-aged female mice requires dorsal hippocampal extracellular signal-regulated kinase and phosphatidylinositol 3-kinase activation. J Neurosci 30:4390–4400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez SM, Lewis MC, Pechenino AS, Harburger LL, Orr PT, Gresack JE, Schafe GE, Frick KM (2008) Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J Neurosci 28:8660–8667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer DK, Rice RC, Martinez Rivera A, Donohoe M, Rajadhyaksha AM (2017) Altered reward sensitivity in female offspring of cocaine-exposed fathers. Behav Brain Res 332:23–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forwood SE, Winters BD, Bussey TJ (2005) Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15:347–355

    Article  CAS  PubMed  Google Scholar 

  • Gervais NJ, Jacob S, Brake WG, Mumby DG (2013) Systemic and intra-rhinal-cortical 17-β estradiol administration modulate object-recognition memory in ovariectomized female rats. Horm Behav 64:642–652

    Article  CAS  PubMed  Google Scholar 

  • Gervais NJ, Hamel LM, Brake WG, Mumby DG (2016) Intra-perirhinal cortex administration of estradiol, but not an ERβ agonist, modulates object-recognition memory in ovariectomized rats. Neurobiol Learn Mem 133:89–99

    Article  CAS  PubMed  Google Scholar 

  • Goldberg LR, Gould TJ (2018) Multigenerational and transgenerational effects of paternal exposure to drugs of abuse on behavioral and neural function. Eur J Neurosci

  • Gruene TM, Flick K, Stefano A, Shea SD, Shansky RM (2015) Sexually divergent expression of active and passive conditioned fear responses in rats. Elife 4

  • Handa RJ, Burgess LH, Kerr JE, O’Keefe JA (1994) Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 28:464–476

    Article  CAS  PubMed  Google Scholar 

  • He F, Lidow IA, Lidow MS (2006) Consequences of paternal cocaine exposure in mice. Neurotoxicol Teratol 28:198–209

    Article  CAS  PubMed  Google Scholar 

  • Jacome LF, Gautreaux C, Inagaki T, Mohan G, Alves S, Lubbers LS, Luine V (2010) Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines. Neurobiol Learn Mem 94:488–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins TG, Carrell DT (2012) The sperm epigenome and potential implications for the developing embryo. Reproduction 143:727–734

    Article  CAS  PubMed  Google Scholar 

  • Kaati G, Bygren LO, Edvinsson S (2002) Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur J Hum Genet 10:682–688

    Article  CAS  PubMed  Google Scholar 

  • Killinger CE, Robinson S, Stanwood GD (2012) Subtle biobehavioral effects produced by paternal cocaine exposure. Synapse 66:902–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Szinte JS, Boulware MI, Frick KM (2016) 17β-Estradiol and agonism of G-protein-coupled estrogen receptor enhance hippocampal memory via different cell-signaling mechanisms. J Neurosci 36:3309–3321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koss WA, Haertel JM, Philippi SM, Frick KM (2018) Sex differences in the rapid cell signaling mechanisms underlying the memory-enhancing effects of 17β-estradiol. eNeuro 5

  • Kudielka BM, Kirschbaum C (2005) Sex differences in HPA axis responses to stress: a review. Biol Psychol 69:113–132

    Article  PubMed  Google Scholar 

  • Kuroki Y, Fukushima K, Kanda Y, Mizuno K, Watanabe Y (2000) Putative membrane-bound estrogen receptors possibly stimulate mitogen-activated protein kinase in the rat hippocampus. Eur J Pharmacol 400:205–209

    Article  CAS  PubMed  Google Scholar 

  • Le Q, Yan B, Yu X, Li Y, Song H, Zhu H, Hou W, Ma D, Wu F, Zhou Y, Ma L (2017) Drug-seeking motivation level in male rats determines offspring susceptibility or resistance to cocaine-seeking behaviour. Nat Commun 8:15527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Wu CF, Pei G, Xu NJ (2001) Reversal of morphine-induced memory impairment in mice by withdrawal in Morris water maze: possible involvement of cholinergic system. Pharmacol Biochem Behav 68:507–513

    Article  CAS  PubMed  Google Scholar 

  • Li CQ, Luo YW, Bi FF, Cui TT, Song L, Cao WY, Zhang JY, Li F, Xu JM, Hao W, Xing XW, Zhou FH, Zhou XF, Dai RP (2014) Development of anxiety-like behavior via hippocampal IGF-2 signaling in the offspring of parental morphine exposure: effect of enriched environment. Neuropsychopharmacology 39:2777–2787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim JP, Brunet A (2013) Bridging the transgenerational gap with epigenetic memory. Trends Genet 29:176–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin CS, Tao PL, Jong YJ, Chen WF, Yang CH, Huang LT, Chao CF, Yang SN (2009) Prenatal morphine alters the synaptic complex of postsynaptic density 95 with N-methyl-D-aspartate receptor subunit in hippocampal CA1 subregion of rat offspring leading to long-term cognitive deficits. Neuroscience 158:1326–1337

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Bilkey DK (1998) Excitotoxic lesions centered on perirhinal cortex produce delay-dependent deficits in a test of spatial memory. Behav Neurosci 112:512–524

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Bilkey DK (2001) The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behav Neurosci 115:94–111

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Wu XY, Zhu QB, Li J, Shi LG, Wu JL, Zhang QJ, Huang ML, Bao AM (2015) Sex differences in the stress response in SD rats. Behav Brain Res 284:231–237

    Article  CAS  PubMed  Google Scholar 

  • Lymer J, Robinson A, Winters BD, Choleris E (2017) Rapid effects of dorsal hippocampal G-protein coupled estrogen receptor on learning in female mice. Psychoneuroendocrinology 77:131–140

    Article  CAS  PubMed  Google Scholar 

  • Mitchnick KA, Mendell AL, Wideman CE, Jardine KH, Creighton SD, Muller AM, Choleris E, MacLusky NJ, Winters BD (2019) Dissociable involvement of estrogen receptors in perirhinal cortex-mediated object-place memory in male rats. Psychoneuroendocrinology 107:98–108

    Article  CAS  PubMed  Google Scholar 

  • Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201–206

    Article  CAS  PubMed  Google Scholar 

  • Morgan CP, Bale TL (2011) Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 31:11748–11755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moulaei N, Mondanizadeh M, Salmani ME, Palizvan MR, Khansarinejad B, Sadegh M (2018) Transgenerational consequences of prepregnancy chronic morphine use on spatial learning and hippocampal Mecp2 and Hdac2 expression. Neuroreport 29:739–744

    Article  CAS  PubMed  Google Scholar 

  • Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H (2002) Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 9:49–57

    Article  PubMed  PubMed Central  Google Scholar 

  • Narkowicz S, Płotka J, Polkowska Ż, Biziuk M, Namieśnik J (2013) Prenatal exposure to substance of abuse: a worldwide problem. Environ Int 54:141–163

    Article  CAS  PubMed  Google Scholar 

  • Nasiraei-Moghadam S, Sherafat MA, Safari MS, Moradi F, Ahmadiani A, Dargahi L (2013) Reversal of prenatal morphine exposure-induced memory deficit in male but not female rats. J Mol Neurosci 50:58–69

    Article  CAS  PubMed  Google Scholar 

  • Oliveira AM, Hawk JD, Abel T, Havekes R (2010) Post-training reversible inactivation of the hippocampus enhances novel object recognition memory. Learn Mem 17:155–160

    Article  PubMed  PubMed Central  Google Scholar 

  • Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14:159–166

    Article  PubMed  Google Scholar 

  • Pereira LM, Bastos CP, de Souza JM, Ribeiro FM, Pereira GS (2014) Estradiol enhances object recognition memory in Swiss female mice by activating hippocampal estrogen receptor α. Neurobiol Learn Mem 114:1–9

    Article  CAS  PubMed  Google Scholar 

  • Phan A, Lancaster KE, Armstrong JN, MacLusky NJ, Choleris E (2011) Rapid effects of estrogen receptor α and β selective agonists on learning and dendritic spines in female mice. Endocrinology 152:1492–1502

    Article  CAS  PubMed  Google Scholar 

  • Phan A, Suschkov S, Molinaro L, Reynolds K, Lymer JM, Bailey CD, Kow LM, MacLusky NJ, Pfaff DW, Choleris E (2015) Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements. Proc Natl Acad Sci U S A 112:16018–16023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pierce RC, Fant B, Swinford-Jackson SE, Heller EA, Berrettini WH, Wimmer ME (2018) Environmental, genetic and epigenetic contributions to cocaine addiction. Neuropsychopharmacology 43:1471–1480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piterkin P, Cole E, Cossette MP, Gaskin S, Mumby DG (2008) A limited role for the hippocampus in the modulation of novel-object preference by contextual cues. Learn Mem 15:785–791

    Article  PubMed  Google Scholar 

  • Ploense KL, Vieira P, Bubalo L, Olivarria G, Carr AE, Szumlinski KK, Kippin TE (2018) Contributions of prolonged contingent and non-contingent cocaine exposure to escalation of cocaine intake and glutamatergic gene expression. Psychopharmacology 235:1347–1359

    Article  CAS  PubMed  Google Scholar 

  • Pooriamehr A, Sabahi P, Miladi-Gorji H (2017) Effects of environmental enrichment during abstinence in morphine dependent parents on anxiety, depressive-like behaviors and voluntary morphine consumption in rat offspring. Neurosci Lett 656:37–42

    Article  CAS  PubMed  Google Scholar 

  • Rabbani M, Hajhashemi V, Mesripour A (2009) Increase in brain corticosterone concentration and recognition memory impairment following morphine withdrawal in mice. Stress 12:451–456

    Article  CAS  PubMed  Google Scholar 

  • Radley JJ, Kabbaj M, Jacobson L, Heydendael W, Yehuda R, Herman JP (2011) Stress risk factors and stress-related pathology: neuroplasticity, epigenetics and endophenotypes. Stress 14:481–497

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL (2013) Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 33:9003–9012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodgers AB, Morgan CP, Leu NA, Bale TL (2015) Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci U S A 112:13699–13704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabzevari S, Rohbani K, Sadat-Shirazi MS, Babhadi-Ashar N, Shakeri A, Ashabi G, Khalifeh S, Ale-Ebrahim M, Zarrindast MR (2018) Morphine exposure before conception affects anxiety-like behavior and CRF level (in the CSF and plasma) in the adult male offspring. Brain Res Bull 144:122–131

    Article  CAS  PubMed  Google Scholar 

  • Saha N, Datta H, Sharma PL (1991) Effects of morphine on memory: interactions with naloxone, propranolol and haloperidol. Pharmacology 42:10–14

    Article  CAS  PubMed  Google Scholar 

  • Sepehri G, Parsania S, Hajzadeh MA, Haghpanah T, Sheibani V, Divsalar K, Shekarforoush S, Afarinesh MR (2014) The effects of co-administration of opium and morphine with nicotine during pregnancy on spatial learning and memory of adult male offspring rats. Iran J Basic Med Sci 17:694–701

    PubMed  PubMed Central  Google Scholar 

  • Sithisarn T, Bada HS, Dai H, Randall DC, Legan SJ (2011) Effects of perinatal cocaine exposure on open field behavior and the response to corticotropin releasing hormone (CRH) in rat offspring. Brain Res 1370:136–144

    Article  CAS  PubMed  Google Scholar 

  • Spencer RL, Deak T (2017) A users guide to HPA axis research. Physiol Behav 178:43–65

    Article  CAS  PubMed  Google Scholar 

  • Tan JW, Duan TT, Zhou QX, Ding ZY, Jing L, Cao J, Wang LP, Mao RR, Xu L (2015) Impaired contextual fear extinction and hippocampal synaptic plasticity in adult rats induced by prenatal morphine exposure. Addict Biol 20:652–662

    Article  CAS  PubMed  Google Scholar 

  • Tuscher JJ, Szinte JS, Starrett JR, Krentzel AA, Fortress AM, Remage-Healey L, Frick KM (2016) Inhibition of local estrogen synthesis in the hippocampus impairs hippocampal memory consolidation in ovariectomized female mice. Horm Behav 83:60–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Twining RC, Bolan M, Grigson PS (2009) Yoked delivery of cocaine is aversive and protects against the motivation for drug in rats. Behav Neurosci 123:913–925

    Article  CAS  PubMed  Google Scholar 

  • Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC (2013) Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16:42–47

    Article  CAS  PubMed  Google Scholar 

  • Vassoler FM, Wright SJ, Byrnes EM (2016) Exposure to opiates in female adolescents alters mu opiate receptor expression and increases the rewarding effects of morphine in future offspring. Neuropharmacology 103:112–121

    Article  CAS  PubMed  Google Scholar 

  • Vassoler FM, Oliver DJ, Wyse C, Blau A, Shtutman M, Turner JR, Byrnes EM (2017) Transgenerational attenuation of opioid self-administration as a consequence of adolescent morphine exposure. Neuropharmacology 113:271–280

    Article  CAS  PubMed  Google Scholar 

  • Vassoler FM, Toorie AM, Byrnes EM (2018a) Increased cocaine reward in offspring of females exposed to morphine during adolescence. Psychopharmacology (Berl)

  • Vassoler FM, Toorie AM, Byrnes EM (2018b) Transgenerational blunting of morphine-induced corticosterone secretion is associated with dysregulated gene expression in male offspring. Brain Res 1679:19–25

    Article  CAS  PubMed  Google Scholar 

  • Watkins AJ, Dias I, Tsuro H, Allen D, Emes RD, Moreton J, Wilson R, Ingram RJM, Sinclair KD (2018) Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proc Natl Acad Sci U S A 115:10064–10069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weise-Kelly L, Siegel S (2001) Self-administration cues as signals: drug self-administration and tolerance. J Exp Psychol Anim Behav Process 27:125–136

    Article  CAS  PubMed  Google Scholar 

  • White SL, Vassoler FM, Schmidt HD, Pierce RC, Wimmer ME (2016) Enhanced anxiety in the male offspring of sires that self-administered cocaine. Addict Biol 21:802–810

    Article  CAS  PubMed  Google Scholar 

  • Wiig KA, Bilkey DK (1994) The effects of perirhinal cortical lesions on spatial reference memory in the rat. Behav Brain Res 63:101–109

    Article  CAS  PubMed  Google Scholar 

  • Wimmer ME, Briand LA, Fant B, Guercio LA, Arreola AC, Schmidt HD, Sidoli S, Han Y, Garcia BA, Pierce RC (2017) Paternal cocaine taking elicits epigenetic remodeling and memory deficits in male progeny. Mol Psychiatry 22:1653

    Article  CAS  PubMed  Google Scholar 

  • Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24:5901–5908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SN, Liu CA, Chung MY, Huang HC, Yeh GC, Wong CS, Lin WW, Yang CH, Tao PL (2006) Alterations of postsynaptic density proteins in the hippocampus of rat offspring from the morphine-addicted mother: beneficial effect of dextromethorphan. Hippocampus 16:521–530

    Article  CAS  PubMed  Google Scholar 

  • Yaw AM, Woodruff RW, Prosser RA, Glass JD (2018) Paternal cocaine disrupts offspring circadian clock function in a sex-dependent manner in mice. Neuroscience 379:257–268

    Article  CAS  PubMed  Google Scholar 

  • Yaw AM, Prosser RA, Jones PC, Garcia BJ, Jacobson DA, Glass JD (2019) Epigenetic effects of paternal cocaine on reward stimulus behavior and accumbens gene expression in mice. Behav Brain Res 367:68–81

    Article  CAS  PubMed  Google Scholar 

  • Yehuda R, Lehrner A (2018) Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms. World Psychiatry 17:243–257

    Article  PubMed  PubMed Central  Google Scholar 

  • Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T, Holsboer F, Binder EB (2016) Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biol Psychiatry 80:372–380

    Article  CAS  PubMed  Google Scholar 

  • Yoburn BC, Chen J, Huang T, Inturrisi CE (1985) Pharmacokinetics and pharmacodynamics of subcutaneous morphine pellets in the rat. J Pharmacol Exp Ther 235:282–286

    CAS  PubMed  Google Scholar 

  • Yohn NL, Bartolomei MS, Blendy JA (2015) Multigenerational and transgenerational inheritance of drug exposure: the effects of alcohol, opiates, cocaine, marijuana, and nicotine. Prog Biophys Mol Biol 118:21–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Proudnikov D, Yuferov V, Kreek MJ (2010) Drug-induced and genetic alterations in stress-responsive systems: implications for specific addictive diseases. Brain Res 1314:235–252

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Zhu H, Wu HY, Jin LY, Chen B, Pang HY, Ming ZH, Cheng Y, Zhou CL, Guo MX, Huang YT, Yu DQ, Sheng JZ, Huang HF (2018) Diet-induced paternal obesity impairs cognitive function in offspring by mediating epigenetic modifications in spermatozoa. Obesity (Silver Spring) 26:1749–1757

    Article  CAS  Google Scholar 

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Funding

This work was supported by the following grant from the National Institutes of Health: DP1 DA046537 (MEW), K01 DA039308 (MEW), T32 DA007237 (ABT; Unterwald EM, PI).

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  1. Department of Psychology and Program in Neuroscience, Temple University, Philadelphia, PA, USA

    Alexandra S. Ellis, Andre B. Toussaint, Melissa C. Knouse, Arthur S. Thomas, Angela R. Bongiovanni, Hannah L. Mayberry, Shivam Bhakta, Kyle Peer, Debra A. Bangasser & Mathieu E. Wimmer

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  1. Alexandra S. Ellis
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  2. Andre B. Toussaint
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  3. Melissa C. Knouse
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  4. Arthur S. Thomas
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Correspondence to Mathieu E. Wimmer.

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Ellis, A.S., Toussaint, A.B., Knouse, M.C. et al. Paternal morphine self-administration produces object recognition memory deficits in female, but not male offspring. Psychopharmacology 237, 1209–1221 (2020). https://doi.org/10.1007/s00213-019-05450-6

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