Annual research review: Epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development
Open accessAbstract
Experiences during early development profoundly affect development of the central nervous system (CNS) to impart either risk for or resilience to later psychopathology. Work in the developmental neuroscience field is providing compelling data that epigenetic marking of the genome may underlie aspects of this process. Experiments in rodents continue to show that experiences during sensitive periods of development influence DNA methylation patterns of several genes. These experience‐induced DNA methylation patterns represent stable epigenetic modifications that alter gene transcription throughout the lifespan and promote specific behavioral outcomes. We discuss the relevance of these findings to humans, and also briefly discuss these findings in the broader contexts of cognition and psychiatric disorder. We conclude by discussing the implications of these observations for future research.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679 · see citing works
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120 · see citing works
DNA methylation patterns and epigenetic memory
Bird, A. (2002) · Genes & Development · doi:10.1101/gad.947102 · Cited by 7,124 · see citing works
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · cited 1× · see citing works
“…adversity , dysregulation of mediators of neural function and plasticity in brain regions such as the prefrontal cortex has also emerged as a leading candidate responsible for the lasting changes in cognition induced by early-life stress (Fumagalli, Molteni, Racagni, & Riva, 2007; McEwen, 2007).”
BackgroundRole of genotype in the cycle of violence in maltreated children
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W., Taylor, A., & Poulton, R. (2002) · Science · doi:10.1126/science.1072290 · Cited by 4,842 · see citing works
Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2270 · Cited by 3,531 · see citing works
A Neurotrophic Model for Stress-Related Mood Disorders
Duman, R. S., & Monteggia, L. M. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.02.013 · Cited by 3,375 · see citing works
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791 · see citing works
The complex language of chromatin regulation during transcription
Berger, S. L. (2007) · Nature · doi:10.1038/nature05915 · Cited by 2,768 · see citing works
Haberland, M., Montgomery, R. L., & Olson, E. N. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2485 · Cited by 2,541 · 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
The neurobiology of stress and development.
Gunnar, M., & Quevedo, K. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085605 · Cited by 2,011 · cited 2× · see citing works
“Akin to the clinical data, rodent and non-human primate models of early-life adversity show that early trauma produces lasting changes in neural function and behavior (e.g., Gunnar & Quevedo, 2007; Kaffman & Meaney, 2007; Korosi & Baram, 2009; Pryce & Feldon, 2003; Sanchez, 2006).”
BackgroundMeCP2, a Key Contributor to Neurological Disease, Activates and Represses Transcription
Chahrour, M., Jung, S. Y., Shaw, C., Zhou, X., Wong, S. T. C., Qin, J., & Zoghbi, H. Y. (2008) · Science · doi:10.1126/science.1153252 · Cited by 1,823 · see citing works
Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action
Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., & Nestler, E. J. (2006) · Nature Neuroscience · doi:10.1038/nn1659 · Cited by 1,780 · see citing works
The neurobiological consequences of early stress and childhood maltreatment
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00007-1 · Cited by 1,465 · see citing works
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432 · see citing works
Epigenetic regulation in psychiatric disorders
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2132 · Cited by 1,400 · see citing works
Perry, B. D., Pollard, R. A., Blakley, T. L., Baker, W. L., & Vigilante, D. (1995) · Infant Mental Health Journal · doi:10.1002/1097-0355(199524)16:4 · Cited by 1,325 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · see citing works
Self-citationRecovery of learning and memory is associated with chromatin remodelling
Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., & Tsai, L.-H. (2007) · Nature · doi:10.1038/nature05772 · Cited by 1,227 · see citing works
Covalent Modification of DNA Regulates Memory Formation
Miller, C. A., & Sweatt, J. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.022 · Cited by 1,180 · see citing works
Dynamic DNA methylation programs persistent adverse effects of early-life stress
Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmühl, Y., Fischer, D., Holsboer, F., Wotjak, C. T., Almeida, O. F. X., & Spengler, D. (2009) · Nature Neuroscience · doi:10.1038/nn.2436 · Cited by 1,162 · see citing works
Gene-environment interplay and psychopathology: multiple varieties but real effects
Rutter, M., Moffitt, T. E., & Caspi, A. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2005.01557.x · Cited by 1,058 · see citing works
Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00149-5 · Cited by 1,021 · see citing works
Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988 · see citing works
Neuronal Activity–Induced Gadd45b Promotes Epigenetic DNA Demethylation and Adult Neurogenesis
Dengke, K., Jang, M., Guo, J. U., Kitabatake, Y., Chang, M.-L., Pow-anpongkul, N., Flavell, R. A., Lu, B., Ming, G., & Song, H. (2009) · Science · doi:10.1126/science.1166859 · Cited by 929 · see citing works
Weaver, I. C. G., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., & Szyf, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3652-05.2005 · Cited by 905 · see citing works
Epigenetic Regulation of <i>bdnf</i> Gene Transcription in the Consolidation of Fear Memory
Lubin, F. D., Roth, T. L., & Sweatt, J. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1786-08.2008 · Cited by 793 · see citing works
Self-citationEpigenomic Profiling Reveals DNA-Methylation Changes Associated with Major Psychosis
Mill, J., Tang, T., Kaminsky, Z., Khare, T., Yazdanpanah, S., Bouchard, L., Jia, P., Assadzadeh, A., Flanagan, J., Schumacher, A., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.01.008 · Cited by 773 · see citing works
Weaver, I. C. G., Meaney, M. J., & Szyf, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507526103 · Cited by 771 · see citing works
Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation
Barreto, G., Schäfer, A., Marhold, J., Stach, D., Swaminathan, S. K., Handa, V., Doederlein, G., Maltry, N., Wu, W., Lyko, F., et al. (2007) · Nature · doi:10.1038/nature05515 · Cited by 753 · see citing works
Champagne, F., Diorio, J., Sharma, S., & Meaney, M. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221224598 · Cited by 707 · see citing works
DNA methylation: The nuts and bolts of repression
Miranda, T. B., & Jones, P. A. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21224 · Cited by 685 · see citing works
Champagne, F. A., Weaver, I. C. G., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006) · Endocrinology · doi:10.1210/en.2005-1119 · Cited by 675 · see citing works
Prenatal stress, glucocorticoids and the programming of adult disease
Cottrell, E. C. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.019.2009 · Cited by 640 · see citing works
A mammalian protein with specific demethylase activity for mCpG DNA
Bhattacharya, S. K., Ramchandani, S., Cervoni, N., & Moshe Szyf, A. (1999) · Nature · doi:10.1038/17533 · Cited by 616 · see citing works
Epigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565 · see citing works
De Bellis, M. D. (2005) · Child Maltreatment · doi:10.1177/1077559505275116 · Cited by 531 · see citing works
Decoding the Epigenetic Language of Neuronal Plasticity
Borrelli, E., Nestler, E. J., Allis, C. D., & Sassone‐Corsi, P. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.012 · Cited by 529 · see citing works
Schore, A. N. (2002) · Australian & New Zealand Journal of Psychiatry · doi:10.1046/j.1440-1614.2002.00996.x · Cited by 528 · see citing works
Effects of early adverse experiences on brain structure and function: clinical implications
Kaufman, J., Plotsky, P. M., Nemeroff, C. B., & Charney, D. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00998-7 · Cited by 508 · see citing works
The Epigenetics of Sex Differences in the Brain: Figure 1.
McCarthy, M. M., Auger, A. P., Bale, T. L., Vries, G. J. D., Dunn, G. A., Forger, N. G., Murray, E. K., Nugent, B. M., Schwarz, J. M., & Wilson, M. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3331-09.2009 · Cited by 478 · see citing works
Pryce, C. R., & Feldon, J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00009-5 · Cited by 460 · see citing works
Impact of Maternal Stress, Depression and Anxiety on Fetal Neurobehavioral Development
KINSELLA, M. T., & MONK, C. (2009) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181b52df1 · Cited by 422 · see citing works
Abdolmaleky, H. M., Cheng, K., Russo, A. L., Smith, C. L., Faraone, S. V., Wilcox, M., Shafa, R., Glatt, S. J., Nguyen, G. H., Ponte, J. F., et al. (2005) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30140 · Cited by 390 · see citing works
Kaffman, A., & Meaney, M. J. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01730.x · Cited by 385 · see citing works
Yasui, D. H., Peddada, S., Bieda, M. C., Vallero, R. O., Hogart, A., Nagarajan, R. P., Thatcher, K. N., Farnham, P., & LaSalle, J. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707442104 · Cited by 381 · see citing works
Francis, D. D., Caldji, C., Champagne, F., Plotsky, P. M., & Meaney, M. J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00237-1 · Cited by 380 · see citing works
Epigenetic influences on brain development and plasticity
Fagiolini, M., Jensen, C. L., & Champagne, F. A. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.009 · Cited by 362 · see citing works
Histone modifying enzymes: Structures, mechanisms, and specificities
Marmorstein, R., & Trievel, R. C. (2008) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2008.07.009 · Cited by 325 · see citing works
Good memories of bad events in infancy
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000) · Nature · doi:10.1038/35024156 · Cited by 315 · see citing works
Epigenetic codes in cognition and behaviour
Gräff, J., & Mansuy, I. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.01.021 · Cited by 307 · see citing works
The epigenetics of social adversity in early life: Implications for mental health outcomes
McGowan, P. O., & Szyf, M. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.12.026 · Cited by 272 · see citing works
Meaney, M. J., Diorio, J., Francis, D., Weaver, S., Yau, J., Chapman, K., & Seckl, J. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03926.2000 · Cited by 266 · see citing works
The impact of early adverse care on HPA axis development: Nonhuman primate models
Sánchez, M. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.012 · Cited by 247 · see citing works
Long-term effects of childhood abuse on brain and neurobiology
Bremner, J. D. (2003) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/s1056-4993(02)00098-6 · Cited by 243 · see citing works
Stress during development: Impact on neuroplasticity and relevance to psychopathology
Fumagalli, F., Molteni, R., Racagni, G., & Riva, M. A. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.01.002 · Cited by 218 · see citing works
Moriceau, S., Shionoya, K., Jakubs, K., & Sullivan, R. M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4106-09.2009 · Cited by 214 · see citing works
Brown, G. W., & Harris, T. (2008) · Journal of Affective Disorders · doi:10.1016/j.jad.2008.04.009 · Cited by 199 · see citing works
Schlinzig, T., Johansson, S., Gunnar, A., Ekström, T. J., & Norman, M. (2009) · Acta Paediatrica · doi:10.1111/j.1651-2227.2009.01371.x · Cited by 184 · see citing works
Examining the Intersection of Sex and Stress in Modelling Neuropsychiatric Disorders
Goel, N., & Bale, T. L. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01843.x · Cited by 182 · see citing works
Epigenetic mechanisms in schizophrenia
Roth, T. L., Lubin, F. D., Sodhi, M., & Kleinman, J. E. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.06.009 · Cited by 168 · see citing works
Self-citationEpigenetic inheritance in mammals: Evidence for the impact of adverse environmental effects
Franklin, T. B., & Mansuy, I. M. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.11.012 · Cited by 153 · see citing works
DNA methylation impacts on learning and memory in aging
Liu, L., van Groen, T., Kadish, I., & Tollefsbol, T. O. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.07.020 · Cited by 152 · see citing works
Novikova, S. I., He, F., Bai, J., Cutrufello, N. J., Lidow, M. S., & Undieh, A. S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001919 · Cited by 140 · see citing works
Regulation of chromatin structure in memory formation
Roth, T. L., & Sweatt, J. D. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.011 · Cited by 138 · see citing works
Self-citationEpigenetic control of neurobehavioural plasticity: the role of neurotrophins
Branchi, I., Francia, N., & Alleva, E. (2004) · Behavioural Pharmacology · doi:10.1097/00008877-200409000-00006 · Cited by 133 · see citing works
Casey, B. J., Glatt, C. E., Tottenham, N., Soliman, F., Bath, K., Amso, D., Altemus, M., Pattwell, S., Jones, R., Levita, L., et al. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.081 · Cited by 129 · see citing works
Transitions in infant learning are modulated by dopamine in the amygdala
Barr, G. A., Moriceau, S., Shionoya, K., Muzny, K., Gao, P., Wang, S., & Sullivan, R. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2403 · Cited by 112 · see citing works
The pathways from mother's love to baby's future
Kőrösi, A. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.027.2009 · Cited by 92 · see citing works
Kumsta, R., Stevens, S., Brookes, K., Schlotz, W., Castle, J., Beckett, C., Kreppner, J., Rutter, M., & Sonuga‐Barke, E. (2010) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02249.x · Cited by 91 · see citing works
DNA methylation changes in schizophrenia and bipolar disorder
Connor, C., & Akbarian, S. (2008) · Epigenetics · doi:10.4161/epi.3.2.5938 · Cited by 84 · see citing works
Costa, E., Chen, Y., Dong, E., Grayson, D. R., Kundaković, M., Maloku, E., Ruzicka, W. B., Satta, R., Veldić, M., Zhubi, A., et al. (2008) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.9.1.87 · Cited by 62 · see citing works
Grayson, D. R., Chen, Y., Dong, E., Kundaković, M., & Guidotti, A. (2009) · Epigenetics · doi:10.4161/epi.4.3.8534 · Cited by 54 · see citing works
Cohen, S., Zhou, Z., & Greenberg, M. E. (2008) · Science · doi:10.1126/science.1159146 · Cited by 46 · see citing works
Gavin, D. P., & Sharma, R. P. (2009) · Cardiovascular Psychiatry and Neurology · doi:10.1155/2009/409562 · Cited by 27 · see citing works
Epigenetic biomarkers in psychiatric disorders
Peedicayil, J. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.254 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation
Yehuda, R., Daskalakis, N. P., Bierer, L. M., Bader, H. N., Klengel, T., Holsboer, F., & Binder, E. B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.005 · Cited by 782 · see citing works
Feldman, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000048 · Cited by 271 · see citing works
Stern, J. A., & Cassidy, J. (2018) · Developmental Review · doi:10.1016/j.dr.2017.09.002 · Cited by 222 · see citing works
Roy, B., Shelton, R. C., & Dwivedi, Y. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.02.005 · Cited by 139 · see citing works
Shumay, E., Logan, J., Volkow, N. D., & Fowler, J. S. (2012) · Epigenetics · doi:10.4161/epi.21976 · Cited by 120 · see citing works
Developmental origins of cardiovascular disease: Impact of early life stress in humans and rodents
Murphy, M. O., Cohn, D. M., & Loria, A. S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.018 · Cited by 117 · see citing works
Goossens, L., van Roekel, E., Verhagen, M., Cacioppo, J. T., Cacioppo, S., Maes, M., & Boomsma, D. I. (2015) · Perspectives on Psychological Science · doi:10.1177/1745691614564878 · Cited by 103 · see citing works
Kofink, D., Boks, M. P. M., Timmers, H. T. M., & Kas, M. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.020 · Cited by 83 · see citing works
Chen, L., Pan, H., Tuan, T. A., Teh, A. L., MacIsaac, J. L., Mah, S. M., McEwen, L. M., Li, Y., Chen, H., Broekman, B. F. P., et al. (2015) · Development and Psychopathology · doi:10.1017/s0954579414001357 · Cited by 75 · see citing works
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
The elusive engram: what can infantile amnesia tell us about memory?
Callaghan, B. L., Li, S., & Richardson, R. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2013.10.007 · Cited by 51 · see citing works
Yang, M., Lewis, F., Foley, G., & Crawley, J. N. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.023 · Cited by 28 · see citing works
Rothenberger, L. G. (2012) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32111 · Cited by 8 · see citing works
- Authors
- Roth, T. L., & David Sweatt, J.
- Affiliations
- University of Alabama at Birmingham (US)
- ORCID
- Roth, Tania L.
- Venue
- Journal of Child Psychology and Psychiatry
- Publisher
- Wiley
- Published
- 2011-03-15
- Volume
- 52
- Issue
- 4
- Pages
- 398-408
- ISSN
- 0021-9630 (ISSN-L)
- 1469-7610
- PMC
- PMC2965301
- OpenAlex
- W2106201573
- Cited by
- 246
- References
- 81
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 4 · 2023: 7 · 2022: 7 · 2021: 13 · 2020: 11 · 2019: 17 · 2018: 23 · 2017: 25 · 2016: 32 · 2015: 26 · 2014: 16 · 2013: 23 · 2012: 18
- FWCI
- 1.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Child Psychology and Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (R01AG031722)
- National Institute of Mental Health (R01MH057014)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Keywords
- epigenetics, DNA methylation, sensitive periods of development, early life experience, brain development, central nervous system development, gene transcription, behavioral effects, cognitive development, mental illness, rodent models
- MeSH terms
- Animals, Mental Disorders, Brain, Cognition Disorders, Female, Gene Expression Regulation, Histones, Humans, Infant, Newborn, Life Change Events, Maternal Behavior, Pregnancy, Prenatal Exposure Delayed Effects, Social Environment, Transcription, Genetic, Epigenesis, Genetic, Mice, Rats, Resilience, Psychological
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review