Multigenerational and transgenerational effects of paternal exposure to drugs of abuse on behavioral and neural function
Open accessAbstract
Addictions are highly heritable disorders, with heritability estimates ranging from 39% to 72%. Multiple studies suggest a link between paternal drug abuse and addiction in their children. However, patterns of inheritance cannot be explained purely by Mendelian genetic mechanisms. Exposure to drugs of abuse results in epigenetic changes that may be passed on through the germline. This mechanism of epigenetic transgenerational inheritance may provide a link between paternal drug exposure and addiction susceptibility in the offspring. Recent studies have begun to investigate the effect of paternal drug exposure on behavioral and neurobiological phenotypes in offspring of drug‐exposed fathers in rodent models. This review aims to discuss behavioral and neural effects of paternal exposure to alcohol, cocaine, opioids, and nicotine. Although a special focus will be on addiction‐relevant behaviors, additional behavioral effects including cognition, anxiety, and depressive‐like behaviors will be discussed.
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Cites
Finding the missing heritability of complex diseases
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., et al. (2009) · Nature · doi:10.1038/nature08494 · Cited by 8,336 · see citing works
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,460 · see citing works
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · see citing works
Bird, A. (2007) · Nature · doi:10.1038/nature05913 · Cited by 3,011 · see citing works
Grant, B. F., Goldstein, R. B., Saha, T. D., Chou, S. P., Jung, J., Zhang, H., Pickering, R. P., Ruan, W. J., Smith, S. M., Huang, B., et al. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.0584 · Cited by 2,556 · see citing works
Genomic DNA methylation: the mark and its mediators.
Klose, R. J., & Bird, A. P. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2005.12.008 · Cited by 2,501 · see citing works
Environmental epigenomics and disease susceptibility
Jirtle, R. L., & Skinner, M. K. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2045 · Cited by 2,492 · see citing works
Chronic stress, drug use, and vulnerability to addiction
Sinha, R. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1441.030 · Cited by 1,904 · see citing works
Chromatin modification and epigenetic reprogramming in mammalian development
Li, E. (2002) · Nature Reviews Genetics · doi:10.1038/nrg887 · Cited by 1,900 · see citing works
Cloninger, C. R. (1981) · Archives of General Psychiatry · doi:10.1001/archpsyc.1981.01780330019001 · Cited by 1,858 · see citing works
Missing heritability and strategies for finding the underlying causes of complex disease
Eichler, E. E., Flint, J., Gibson, G. C., Kong, A., Leal, S. M., Moore, J. H., & Nadeau, J. H. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2809 · Cited by 1,671 · see citing works
How does stress increase risk of drug abuse and relapse?
Sinha, R. (2001) · Psychopharmacology · doi:10.1007/s002130100917 · Cited by 1,505 · see citing works
Inherited epigenetic variation — revisiting soft inheritance
Richards, E. J. (2006) · Nature reviews genetics · doi:10.1038/nrg1834 · Cited by 1,200 · see citing works
Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling
Lüscher, C., & Malenka, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.017 · Cited by 1,105 · see citing works
The dopamine hypothesis of the reinforcing properties of cocaine
Kuhar, M. J., Ritz, M. C., & Boja, J. W. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90141-g · Cited by 989 · see citing works
The many faces of insulin-like peptide signalling in the brain
Fernandez, A. M., & Torres-Alemán, I. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3209 · Cited by 872 · see citing works
Neurobiology of attention-deficit hyperactivity disorder
Faraone, S. V., & Biederman, J. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00240-6 · Cited by 811 · see citing works
Chromatin Remodeling Is a Key Mechanism Underlying Cocaine-Induced Plasticity in Striatum
Kumar, A., Choi, K.-H., Renthal, W., Tsankova, N. M., Theobald, D. E. H., Truong, H.-T., Russo, S. J., LaPlant, Q., Sasaki, T. S., Whistler, K. N., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.023 · Cited by 764 · see citing works
Epigenetic transgenerational actions of environmental factors in disease etiology
Skinner, M. K., Manikkam, M., & Guerrero‐Bosagna, C. (2010) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.12.007 · Cited by 713 · see citing works
The scientific case that nicotine is addictive
Stolerman, I. P., & Jarvis, M. J. (1995) · Psychopharmacology · doi:10.1007/bf02245088 · Cited by 646 · see citing works
Corticosterone levels determine individual vulnerability to amphetamine self-administration.
Piazza, P. V., Maccari, S., Deminière, J.-M., Moal, M. L., Mormède, P., & Simon, H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.6.2088 · Cited by 567 · see citing works
What is an epigenetic transgenerational phenotype?
Skinner, M. K. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.09.001 · Cited by 485 · see citing works
Heikkila, R. E., Orlansky, H., & Cohen, G. (1975) · Biochemical Pharmacology · doi:10.1016/0006-2952(75)90152-5 · Cited by 468 · see citing works
Epigenetic mechanisms of drug addiction
Nestler, E. J. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.004 · Cited by 458 · see citing works
Transgenerational transmission of environmental information in <i>C. elegans</i>
Klosin, A., Casas, E., Hidalgo-Carcedo, C., Vavouri, T., & Lehner, B. (2017) · Science · doi:10.1126/science.aah6412 · Cited by 456 · see citing works
Manikkam, M., Guerrero‐Bosagna, C., Tracey, R., Haque, M. M., & Skinner, M. K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031901 · Cited by 451 · see citing works
Epigenetic Transgenerational Actions of Vinclozolin on Promoter Regions of the Sperm Epigenome
Guerrero‐Bosagna, C., Settles, M. L., Lucker, B. F., & Skinner, M. K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013100 · Cited by 427 · see citing works
Epigenetic inheritance of a cocaine-resistance phenotype
Vassoler, F. M., White, S., Schmidt, H. D., Sadri‐Vakili, G., & Pierce, R. C. (2012) · Nature Neuroscience · doi:10.1038/nn.3280 · Cited by 419 · see citing works
Mishra, A., Chaturvedi, P., Datta, S., Sinukumar, S., Joshi, P., & Garg, A. (2015) · Indian Journal of Medical and Paediatric Oncology · doi:10.4103/0971-5851.151771 · Cited by 413 · see citing works
Volkow, N. D., Wang, G.-J., Fowler, J. S., Logan, J., Gatley, S. J., Gifford, A., Hitzemann, R., Ding, Y.-S., & Pappas, N. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.9.1440 · Cited by 406 · see citing works
Volkow, N. D., Wang, G.-J., Fowler, J. S., Hitzemann, R., Angrist, B., Gatley, S. J., Logan, J., Ding, Y.-S., & Pappas, N. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.1.19 · Cited by 405 · see citing works
Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability
(2011) · Epigenetics · doi:10.4161/epi.6.7.16537 · Cited by 368 · see citing works
Abnormalities of the Corpus Callosum in Children Prenatally Exposed to Alcohol
Riley, E. P., Mattson, S. N., Sowell, E. R., Jernigan, T. L., Sobel, D. F., & Jones, K. L. (1995) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1995.tb01600.x · Cited by 345 · see citing works
Heritability of Smoking Initiation and Nicotine Dependence
Vink, J. M., Willemsen, G. A. H. M., & Boomsma, D. I. (2005) · Behavior Genetics · doi:10.1007/s10519-004-1327-8 · Cited by 342 · see citing works
A Study of Alcoholism in Half Siblings
Schuckit, M. A., Goodwin, D. A., & Winokur, G. (1972) · American Journal of Psychiatry · doi:10.1176/ajp.128.9.1132 · Cited by 336 · see citing works
Calcaterra, S., Glanz, J., & Binswanger, I. A. (2013) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.11.018 · Cited by 330 · see citing works
Hu, M., Davies, M., & Kandel, D. B. (2005) · American Journal of Public Health · doi:10.2105/ajph.2004.057232 · Cited by 321 · see citing works
Modeling stress and drug craving in the laboratory: implications for addiction treatment development
Sinha, R. (2009) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00134.x · Cited by 314 · see citing works
The Genetic Basis of Addictive Disorders
Ducci, F., & Goldman, D. (2012) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2012.03.010 · Cited by 303 · see citing works
Circadian blood nicotine concentrations during cigarette smoking
Benowitz, N. L., Kuyt, F., & Jacob, P. (1982) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.1982.233 · Cited by 292 · see citing works
Manikkam, M., Tracey, R., Guerrero‐Bosagna, C., & Skinner, M. K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046249 · Cited by 284 · see citing works
A Decrease in the Size of the Basal Ganglia in Children with Fetal Alcohol Syndrome
Mattson, S. N., Riley, E. P., Sowell, E. R., Jernigan, T. L., Sobel, D. F., & Jones, K. L. (1996) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1996.tb01951.x · Cited by 265 · see citing works
Gender-related differences in the antinociceptive properties of morphine.
Cicero, T. J., Nock, B. L., & Meyer, E. R. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)21187-9 · Cited by 263 · see citing works
Magnetic Resonance Imaging of Brain Anomalies in Fetal Alcohol Syndrome
Swayze, V. W., Johnson, V. P., Hanson, J. W., Piven, J., Satō, Y., Giedd, J. N., Mosnik, D. M., & Andreasen, N. C. (1997) · PEDIATRICS · doi:10.1542/peds.99.2.232 · Cited by 257 · see citing works
Spreading of silent chromatin: inaction at a distance
Talbert, P. B., & Henikoff, S. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1920 · Cited by 245 · see citing works
Dopamine uptake: A review of progress in the last decade
Horn, A. S. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90033-d · Cited by 230 · see citing works
Neurocircuitry of alcohol addiction
Koob, G. F. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-62619-6.00003-3 · Cited by 227 · see citing works
Manikkam, M., Tracey, R., Guerrero‐Bosagna, C., & Skinner, M. K. (2012) · Reproductive Toxicology · doi:10.1016/j.reprotox.2012.08.010 · Cited by 213 · see citing works
Blank, T., Nijholt, I. M., Eckart, K., & Spiess, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03788.2002 · Cited by 210 · see citing works
Bruchas, M. R., Land, B. B., Lemos, J. C., & Chavkin, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008528 · Cited by 204 · see citing works
Szutorisz, H., DiNieri, J. A., Sweet, E. S., Egervári, G., Michaelides, M., Carter, J. M., Ren, Y., Miller, M. L., Blitzer, R. D., & Hurd, Y. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.352 · Cited by 197 · see citing works
Ornoy, A., & Ergaz, Z. (2010) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph7020364 · Cited by 188 · see citing works
A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats
Berglind, W. J., See, R. E., Fuchs, R. A., Ghee, S. M., Whitfield, T. W., Miller, S. W., & McGinty, J. F. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05692.x · Cited by 187 · see citing works
Watson, C. T., Szutorisz, H., Garg, P., Martin, Q., Landry, J. A., Sharp, A. J., & Hurd, Y. L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.155 · Cited by 184 · see citing works
Zangen, A., Nakash, R., Overstreet, D. H., & Yadid, G. (2001) · Psychopharmacology · doi:10.1007/s002130100746 · Cited by 177 · see citing works
Averitt, D. L., Wang, X., & Murphy, A. Z. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4123-08.2008 · Cited by 177 · see citing works
Cicero, T. J., Nock, B. L., & Meyer, E. R. (1997) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)36831-4 · Cited by 174 · see citing works
Gelernter, J. E., Sherva, R., Koesterer, R., Almasy, L. A., Zhao, H., Kranzler, H. R., & Farrer, L. A. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.99 · Cited by 174 · see citing works
Substance use during pregnancy: time for policy to catch up with research
Lester, B. M., Andreozzi, L. M., & Appiah, L. (2004) · Harm Reduction Journal · doi:10.1186/1477-7517-1-5 · Cited by 173 · see citing works
Inherited predisposition to alcoholism: characteristics of sons of male alcoholics
Pihl, R. O., Peterson, J., & Finn, P. R. (1990) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.99.3.291 · Cited by 172 · see citing works
Barrett, S. P., Boileau, I., Okker, J., Pihl, R. O., & Dagher, A. (2004) · Synapse · doi:10.1002/syn.20066 · Cited by 172 · see citing works
Dorsal vs Ventral Hippocampal Neurogenesis: Implications for Cognition and Mood
Kheirbek, M. A., & Hen, R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.148 · Cited by 140 · see citing works
Parent and Child Cigarette Use: A Longitudinal, Multigenerational Study
Vuolo, M., & Staff, J. (2013) · PEDIATRICS · doi:10.1542/peds.2013-0067 · Cited by 139 · see citing works
Bliss, T. V. P., & Lømo, T. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010273 · Cited by 135 · see citing works
Zhao-Shea, R., Liu, L., Pang, X., Gardner, P. D., & Tapper, A. R. (2013) · Current Biology · doi:10.1016/j.cub.2013.09.041 · Cited by 129 · see citing works
Finegersh, A., & Homanics, G. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099078 · Cited by 129 · see citing works
Wnt2 Expression and Signaling Is Increased by Different Classes of Antidepressant Treatments
Okamoto, H., Voleti, B., Banasr, M., Sarhan, M., Đurić, V., Girgenti, M. J., Dileone, R., Newton, S. S., & Duman, R. S. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.023 · Cited by 116 · see citing works
Environmental Signals and Transgenerational Epigenetics
Skinner, M. K., & Guerrero‐Bosagna, C. (2009) · Epigenomics · doi:10.2217/epi.09.11 · Cited by 112 · see citing works
BYRNES, J. J., Babb, J. A., Scanlan, V. F., & Byrnes, E. M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.059 · Cited by 111 · see citing works
Consequences of paternal cocaine exposure in mice
He, F., Lidow, I. A., & Lidow, M. S. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2005.12.003 · Cited by 108 · see citing works
Liang, F., Diao, L., Liu, J., Jiang, N., Zhang, J., Wang, H., Zhou, W., Huang, G., & Ma, D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.025 · Cited by 105 · see citing works
Kim, P., Choi, C. S., Park, J. H., Joo, S. H., Kim, S. Y., Ko, H. M., Kim, K. C., Jeon, S. J., Park, S. H., Han, S., et al. (2014) · Journal of Neuroscience Research · doi:10.1002/jnr.23275 · Cited by 100 · see citing works
The Neuronal Pathways Mediating the Behavioral and Addictive Properties of Nicotine
Balfour, D. J. K. (2009) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-540-69248-5_8 · Cited by 99 · see citing works
Epigenetics: The sins of the father
HUGHES, V. A. (2014) · Nature · doi:10.1038/507022a · Cited by 99 · see citing works
Chatterjee, M., Jaiswal, M., & Palit, G. (2012) · ISRN Psychiatry · doi:10.5402/2012/595141 · Cited by 98 · see citing works
Sex differences in analgesic, reinforcing, discriminative, and motoric effects of opioids.
Craft, R. M. (2008) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0012931 · Cited by 97 · see citing works
Mechanisms of transgenerational inheritance of addictive-like behaviors
Vassoler, F. M., & Sadri-Vakili, G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.064 · Cited by 96 · see citing works
Ventral tegmental site of opiate reward: Antagonism by a hydrophilic opiate receptor blocker
Britt, M. D., & Wise, R. (1983) · Brain Research · doi:10.1016/0006-8993(83)91232-5 · Cited by 93 · see citing works
Alcoholic Fathering and Its Relation to Child's Intellectual Development: A Pilot Investigation
Ervin, C. S., Little, R. E., Streissguth, A. P., et al. (1984) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1984.tb05681.x · Cited by 90 · see citing works
Breaking Barriers in the Genomics and Pharmacogenetics of Drug Addiction
Ho, M., Goldman, D. A., Heinz, A., Kaprio, J. A., Kreek, M. J., Li, M. D., Munafo, M. R., & Tyndale, R. F. (2010) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2010.175 · Cited by 88 · see citing works
Malanga, C. J., & Kosofsky, B. E. (2003) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.09.019 · Cited by 88 · see citing works
Paternal Alcohol Exposure Affects Offspring Behavior but not Body or Organ Weights in Mice
Abel, E. L., & Lee, J. A. (1988) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1988.tb00205.x · Cited by 87 · see citing works
Barker, J. M., Taylor, J. R., Vries, T. J. D., & Peters, J. (2014) · Brain Research · doi:10.1016/j.brainres.2014.10.058 · Cited by 86 · see citing works
Analgesia and the neural substrate of reward
Franklin, K. B. J. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80024-7 · Cited by 84 · see citing works
Le, Q., Yan, B., Yu, X., Li, Y., Song, H., Zhu, H., Hou, W., Ma, D., Wu, F., Zhou, Y., et al. (2017) · Nature Communications · doi:10.1038/ncomms15527 · Cited by 84 · see citing works
Rompala, G. R., Finegersh, A., Slater, M., & Homanics, G. E. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.11.001 · Cited by 83 · see citing works
Environmental, genetic and epigenetic contributions to cocaine addiction
Pierce, R. C., Fant, B., Swinford-Jackson, S. E., Heller, E. A., Berrettini, W. H., & Wimmer, M. E. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0008-x · Cited by 82 · see citing works
Prenatal opiate exposure: long-term CNS consequences in the stress system of the offspring
Vathy, I. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00049-x · Cited by 81 · see citing works
Multigenerational effects of adolescent morphine exposure on dopamine D2 receptor function
BYRNES, J. J., Johnson, N. L., Carini, L. M., et al. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2960-1 · Cited by 81 · see citing works
The Roles of Neurotrophic Factor and Wnt Signaling in Depression
Voleti, B., & Duman, R. S. (2011) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2011.296 · Cited by 78 · see citing works
Byrnes, E. M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0122-4 · Cited by 77 · see citing works
Analgesia and Abuse Potential: An Accidental Association or a Common Substrate?
Franklin, K. B. J. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00535-2 · Cited by 77 · see citing works
Paternal nicotine exposure alters hepatic xenobiotic metabolism in offspring
Vallaster, M., Kukreja, S., Bing, X., Ngolab, J., Zhao-Shea, R., Gardner, P. D., Tapper, A. R., & Rando, O. J. (2017) · eLife · doi:10.7554/elife.24771 · Cited by 75 · see citing works
Abel, E. L., Moore, C., Waselewsky, D. R., Zajac, C. S., & Russell, L. D. (1989) · Journal of Andrology · doi:10.1002/j.1939-4640.1989.tb00051.x · Cited by 71 · see citing works
Li, C.-Q., Luo, Y., Bi, F., Cui, T.-T., Song, L., Cao, W.-Y., Zhang, J. J., Li, F., Xu, J., Hao, W., et al. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.128 · Cited by 71 · see citing works
Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring
Wozniak, D. F., Cicero, T. J., Kettinger, L. A., & Meyer, E. R. (1991) · Psychopharmacology · doi:10.1007/bf02244324 · Cited by 71 · see citing works
Paternal cocaine taking elicits epigenetic remodeling and memory deficits in male progeny
Wimmer, M. E., Briand, L. A., Fant, B., Guercio, L. A., Arreola, A. C., Schmidt, H. D., Sidoli, S., Han, Y., Garcia, B. A., & Pierce, R. C. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.8 · Cited by 70 · see citing works
The antidepressant roles of Wnt2 and Wnt3 in stress-induced depression-like behaviors
Zhou, W.-J., Xu, N., Kong, L., Sun, S.-C., Xu, X.-F., Jia, M.-Z., Wang, Y., & Chen, Z.-Y. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.122 · Cited by 70 · see citing works
Johnson, N. L., Carini, L. M., Schenk, M. E., Stewart, M., & Byrnes, E. M. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00029 · Cited by 67 · see citing works
Cicero, T. J., Adams, M. L., Giordano, A., Miller, B. T., O’Connor, L. H., & Nock, B. L. (1990) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)23128-7 · Cited by 67 · see citing works
Collo, G., Cavalleri, L., & Spano, P. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00259 · Cited by 66 · see citing works
Intergenerational Patterns of Smoking and Nicotine Dependence Among US Adolescents
Kandel, D. B., Griesler, P. C., & Hu, M. (2015) · American Journal of Public Health · doi:10.2105/ajph.2015.302775 · Cited by 66 · see citing works
Petraschka, M., Li, S., Gilbert, T. L., Westenbroek, R. E., Bruchas, M. R., Schreiber, S., Lowe, J. A., III, Low, M. J., Pintar, J. E., & Chavkin, C. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.03.029 · Cited by 63 · see citing works
Observed transition from opioid analgesic deaths toward heroin
Dasgupta, N., Creppage, K. E., Austin, A. E., et al. (2014) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2014.10.005 · Cited by 63 · see citing works
Allen, R. M., Everett, C. V., Nelson, A. M., et al. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.005 · Cited by 62 · see citing works
Johnson, E. O., Chen, L., Breslau, N., Hatsukami, D. K., Robbins, T., Saccone, N. L., Grucza, R. A., & Bierut, L. J. (2010) · Addiction · doi:10.1111/j.1360-0443.2010.03074.x · Cited by 62 · see citing works
Acute paternal alcohol use affects offspring development and adult behavior
Meek, L. R., Myren, K., Sturm, J., & Burau, D. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.02.004 · Cited by 60 · see citing works
Enhanced anxiety in the male offspring of sires that self-administered cocaine
White, S., Vassoler, F. M., Schmidt, H. D., Pierce, R. C., & Wimmer, M. E. (2015) · Addiction Biology · doi:10.1111/adb.12258 · Cited by 59 · see citing works
Subtle biobehavioral effects produced by paternal cocaine exposure
Killinger, C. E., Robinson, S. L., & Stanwood, G. D. (2012) · Synapse · doi:10.1002/syn.21582 · Cited by 59 · see citing works
Vassoler, F. M., Oliver, D. J., Wyse, C., Blau, A., Shtutman, M. S., Turner, J. R., & Byrnes, E. M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.10.006 · Cited by 59 · see citing works
Dai, J., Wang, Z., Xu, W., Zhang, M., Zhu, Z., Zhao, X., Zhang, D., Nie, D., Wang, L., & Qiao, Z. (2017) · Scientific Reports · doi:10.1038/s41598-017-07920-3 · Cited by 58 · see citing works
Carpenter, R. E., Korzan, W. J., Bockholt, C., Watt, M. J., Forster, G. L., Renner, K. J., & Summers, C. H. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.014 · Cited by 57 · see citing works
Effect of parental morphine addiction on hippocampal long-term potentiation in rats offspring
Sarkaki, A., Assaei, R., Motamedi, F., Badavi, M., & Pajouhi, N. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.07.041 · Cited by 57 · see citing works
Information processing, neuropsychological function, and the inherited predisposition to alcoholism
Peterson, J. B., & Pihl, R. O. (1990) · Neuropsychology Review · doi:10.1007/bf01109029 · Cited by 55 · see citing works
Neurobehavioral effects in rat pups whose sires were exposed to alcohol
Jamerson, P. A., Wulser, M. J., & Kimler, B. F. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.12.010 · Cited by 54 · see citing works
Rompala, G. R., Finegersh, A., & Homanics, G. E. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.03.006 · Cited by 53 · see citing works
Vassoler, F. M., Wright, S. J., & Byrnes, E. M. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.11.026 · Cited by 52 · see citing works
Consequences of prenatal substance use
Sithisarn, T., Granger, D. T., & Bada, H. S. (2011) · International Journal of Adolescent Medicine and Health · doi:10.1515/ijamh.2012.016 · Cited by 52 · see citing works
Szutorisz, H., Egervári, G., Sperry, J., Carter, J. M., & Hurd, Y. L. (2016) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2016.05.005 · Cited by 52 · see citing works
Ozkaragoz, T. Z., Satz, P., & Noble, E. P. (1997) · Alcohol · doi:10.1016/s0741-8329(96)00084-5 · Cited by 50 · see citing works
Paternal alcohol exposure and hyperactivity in rat offspring: Effects of amphetamine
Abel, E. L. (1993) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(93)90063-t · Cited by 49 · see citing works
Yuan, T., Li, A., Sun, X., Ouyang, H., Campos, C., Rocha, N., Arias-Carrión, Ó., Machado, S. E. D. C., Hou, G., & So, K. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9526-2 · Cited by 45 · see citing works
A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice
Martini, M., & Valverde, O. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2385-2 · Cited by 43 · see citing works
Altered reward sensitivity in female offspring of cocaine-exposed fathers
Fischer, D. K., Rice, R. C., Martínez-Rivera, A., Donohoe, M. E., & Rajadhyaksha, A. M. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.054 · Cited by 39 · see citing works
CRF2 receptor-deficiency eliminates opiate withdrawal distress without impairing stress coping
Ingallinesi, M., Rouibi, K., Moine, C. L., Papaleo, F., & Contarino, A. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.119 · Cited by 38 · see citing works
A Review of Genome-Wide Association Studies of Stimulant and Opioid Use Disorders
Jensen, K. P. (2016) · Complex Psychiatry · doi:10.1159/000444755 · Cited by 38 · see citing works
Park, P. E., Vendruscolo, L. F., Schlosburg, J. E., Edwards, S., Schulteis, G., & Koob, G. F. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713000308 · Cited by 37 · see citing works
A Critical Role of Brain-Derived Neurotrophic Factor in Alcohol Consumption
Pandey, S. C. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.020 · Cited by 37 · see citing works
Behavioral measures of anxiety during opiate withdrawal
Grasing, K., Wang, A., & Schlussman, S. D. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(96)00035-6 · Cited by 36 · see citing works
South, S. M., Edwards, S. R., & Smith, M. T. (2008) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2008.05019.x · Cited by 35 · see citing works
Cagniard, B., Sotnikova, T. D., Gainetdinov, R. R., & Zhuang, X. (2014) · Journal of Neurogenetics · doi:10.3109/01677063.2014.908191 · Cited by 35 · see citing works
Cicero, T. J., Nock, B. L., O’Connor, L. H., Adams, M. L., & Meyer, E. R. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)09581-3 · Cited by 34 · see citing works
Exposure to opiates in male adolescent rats alters pain perception in the male offspring
Pachenari, N., Azizi, H., Ghasemi, E., Azadi, M., & Semnanian, S. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000388 · Cited by 31 · see citing works
Pooriamehr, A., Sabahi, P., & Miladi‐Gorji, H. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.07.024 · Cited by 30 · see citing works
Vassoler, F. M., Toorie, A. M., & Byrnes, E. M. (2017) · Brain Research · doi:10.1016/j.brainres.2017.11.004 · Cited by 30 · see citing works
Family and Environmental Factors of Drug Addiction among Young Recruits
Jêdrzejczak, M. (2005) · Military Medicine · doi:10.7205/milmed.170.8.688 · Cited by 29 · see citing works
Naquiah, M. Z. F., James, R. J., Suratman, S., et al. (2016) · Behavioral and Brain Functions · doi:10.1186/s12993-016-0107-y · Cited by 29 · see citing works
Heightened aggressive behavior during morphine withdrawal: effects ofd-amphetamine
Tidey, J. W., & Miczek, K. A. (1992) · Psychopharmacology · doi:10.1007/bf02245151 · Cited by 27 · see citing works
Next generation effects of female adolescent morphine exposure
Vassoler, F. M., Johnson-Collins, N. L., Carini, L. M., et al. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000032 · Cited by 26 · see citing works
Genetic factors involved in risk for methamphetamine intake and sensitization
Belknap, J. K., McWeeney, S. K., Reed, C. L., Burkhart‐Kasch, S., McKinnon, C. S., Li, N., Baba, H., Scibelli, A. C., HITZEMANN, R. J., & Phillips, T. J. (2013) · Mammalian Genome · doi:10.1007/s00335-013-9484-9 · Cited by 26 · see citing works
Morisot, N., Monier, R., Moine, C. L., Millan, M. J., & Contarino, A. (2018) · British Journal of Pharmacology · doi:10.1111/bph.14159 · Cited by 26 · see citing works
Effects of Physostigmine on Male Offspring Sired by Alcohol‐Treated Fathers
Abel, E. L. (1994) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1994.tb00925.x · Cited by 25 · see citing works
Preparing the Way: Exploiting Genomic Medicine to Stop Smoking
Bierut, L. J., & Tyndale, R. F. (2018) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.12.001 · Cited by 24 · see citing works
Mandt, B. H., & Zahniser, N. R. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.11.015 · Cited by 21 · see citing works
Morisot, N., Moine, C. L., Millan, M. J., & Contarino, A. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145714000625 · Cited by 21 · see citing works
Umathe, S. N., Mundhada, Y. R., & Bhutada, P. (2012) · Neuropeptides · doi:10.1016/j.npep.2012.06.002 · Cited by 16 · see citing works
Radcliffe, R. A., Bludeau, P., Asperi, W., et al. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0512-2 · Cited by 15 · see citing works
Raivio, N., Miettinen, P. S., & Kiianmaa, K. (2014) · Brain Research · doi:10.1016/j.brainres.2014.07.006 · Cited by 14 · see citing works
Selective breeding for intravenous drug self-administration in rats: a pilot study
He, S., Yang, Y., Mathur, D., & Grasing, K. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32831c3aec · Cited by 12 · see citing works
Behavior and Drug Measurements in Long–Evans and Sprague–Dawley Rats After Ethanol–Cocaine Exposure
Horowitz, J. M., Bhatti, E., Devi, B. G., & Torres, G. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00160-9 · Cited by 9 · see citing works
Frerking, M., & Wilson, M. (1999) · Synapse · doi:10.1002/(sici)1098-2396(19990615)32:4 · Cited by 2 · see citing works
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Nicotine on the developing brain.
Castro, E. M., Lotfipour, S., & Leslie, F. M. (2023) · Pharmacological research · doi:10.1016/j.phrs.2023.106716 · Cited by 140 · see citing works
Drug addiction: from bench to bedside
Cheron, J., & Kerchove d’Exaerde, A. D. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01542-0 · Cited by 75 · see citing works
Of 'junk food' and 'brain food': how parental diet influences offspring neurobiology and behaviour
Bodden, C., Hannan, A. J., & Reichelt, A. C. (2021) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2021.04.001 · Cited by 36 · see citing works
- Authors
- Goldberg, L. R., & Gould, T. J.
- Affiliations
- Pennsylvania State University (US)
- Corresponding author
- Gould, Thomas J.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2018-07-20
- Volume
- 50
- Issue
- 3
- Pages
- 2453-2466
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC7296771
- OpenAlex
- W2811133549
- Cited by
- 88
- References
- 151
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 12 · 2023: 9 · 2022: 15 · 2021: 13 · 2020: 13 · 2019: 13
- FWCI
- 1.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Drug Abuse (U01DA041632)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- paternal drug exposure, transgenerational epigenetic inheritance, alcohol, cocaine, opioids, nicotine, anxiety-like behavior, depression-like behavior, cognition, rodent models
- MeSH terms
- Adult, Brain, Child, Child Behavior Disorders, Humans, Male, Illicit Drugs, Child of Impaired Parents, Paternal Exposure, Substance-Related Disorders, Epigenesis, Genetic
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