Long-term effects of maternal separation coupled with social isolation on reward seeking and changes in dopamine D1 receptor expression in the nucleus accumbens via DNA methylation in mice
Open accessAbstract
Early-life stress has long-lasting effects on the stress response, emotions, and behavior throughout an individual's life. Clinical reports have demonstrated that child abuse victims exhibit impairments in reward-associated behavior; yet, the mechanism for this effect remains unclear. Maternal separation (MS) or MS coupled with social isolation (SI) (MS+SI) is widely used as a model for early-life stress in rodent studies. We employed mice subjected to MS+SI to clarify the long-term effect of early-life stress on reward-seeking involving palatable foods by a conditioned place-preference (CPP) paradigm. Prior MS+SI experience decreased exploration time in a chocolate-paired compartment in adult female mice, but not in male mice. We then focused on the mesolimbic dopamine pathway associated with reward-seeking behavior and measured both mRNA and protein levels of tyrosine hydroxylase (TH) in the ventral tegmental area (VTA) and dopamine D1 and D2 receptors in the nucleus accumbens (NAc). MS+SI female mice had significantly lower D1 receptor mRNA and protein levels than controls, whereas the expression of TH and the D2 receptor was similar in the 2 groups. All mRNA and protein levels were unchanged in MS+SI male mice. When attempting to elucidate the mechanism underlying downregulation of the D1 receptor in the NAc of MS+SI females, we found hypermethylation of the Drd1a promoter region. These results suggest that early-life stress affects reward-seeking behavior in female mice, which may be associated with the downregulation of D1 receptor in the NAc via epigenetic modification of its promoter region.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Maternal separation was associated with decreased conditioned locomotor activity to food-related cues and decreased conditioned place preference to chocolate, indicating decreased reward valuation or incentive salience within approach motivation.
“Maternal separation was also associated with decreased conditioned locomotor activity to food-related cues (Matthews et al., 1996b, 1996a) as well as decreased conditioned place preference to chocolate (Sasagawa et al., 2017) indicative of a decreased reward valuation/incentive salience function within the approach motivation construct.”
From The effects of early life stress on reward processing (2018) · cites this paper as Sasagawa et al., 2017
Cites
1 retracted
Takiguchi, S., Fujisawa, T. X., Mizushima, S., Saito, D. N., Okamoto, Y., Shimada, K., Koizumi, M., Kumazaki, H., Jung, M., Kosaka, H., et al. (2015) · BJPsych Open · doi:10.1192/bjpo.bp.115.001586 · Cited by 63 · see citing works
RetractedThe mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325 · 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
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791 · see citing works
Maternal care as a model for experience-dependent chromatin plasticity?
Meaney, M. J., & Szyf, M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.07.006 · Cited by 658 · see citing works
Hikida, T., Kimura, K., Wada, N., Funabiki, K., & Nakanishi, S. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.011 · Cited by 592 · see citing works
Dopamine Signaling in reward-related behaviors
Baik, J. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00152 · Cited by 534 · see citing works
What's conditioned in conditioned place preference?
Huston, J. P., Silva, M. A. D. S., Topic, B., & Müller, C. P. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.01.004 · Cited by 273 · see citing works
Nishi, M., Horii‐Hayashi, N., & Sasagawa, T. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00166 · Cited by 220 · see citing works
Self-citationEpigenetic marking of the BDNF gene by early-life adverse experiences
Roth, T. L., & Sweatt, J. D. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.05.005 · Cited by 196 · see citing works
Ploj, K., Roman, E., & Nylander, I. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00499-8 · Cited by 192 · see citing works
Matthews, K., Wilkinson, L. S., & Robbins, T. W. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02069-1 · Cited by 178 · see citing works
Hikida, T., Yawata, S., Yamaguchi, T., Danjo, T., Sasaoka, T., Wang, Y., & Nakanishi, S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220358110 · Cited by 120 · see citing works
Epigenetic approaches to psychiatric disorders
Ptak, C., & Petronis, A. (2010) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2010.12.1/cptak · Cited by 118 · see citing works
Visualizing an emotional valence map in the limbic forebrain by TAI-FISH
Xiu, J., Zhang, Q., Zhou, T., Zhou, T.-T., Chen, Y., & Hu, H. (2014) · Nature Neuroscience · doi:10.1038/nn.3813 · Cited by 112 · see citing works
Dexamethasone Treatment Leads to Enhanced Fear Extinction and Dynamic Fkbp5 Regulation in Amygdala
Sawamura, T., Klengel, T., Armario, A., Jovanović, T., Norrholm, S. D., Ressler, K. J., & Andero, R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.210 · Cited by 106 · see citing works
Yang, X., Ewald, E. R., Huo, Y., Tamashiro, K. L., Salvatori, R., Sawa, A., Wand, G. S., & Lee, R. S. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.03.035 · Cited by 97 · see citing works
Matthews, K., Hall, F. S., Wilkinson, L. S., & Robbins, T. W. (1996) · Psychopharmacology · doi:10.1007/bf02246414 · Cited by 93 · see citing works
Dickson, S. L., Hrabovszky, E., Hansson, C., Jerlhag, E., Álvarez-Crespo, M., Skibicka, K. P., Molnar, C. S., Liposits, Z., Engel, J., & Egecioglu, E. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.005 · Cited by 82 · see citing works
Maternal separation is associated with DNA methylation and behavioural changes in adult rats
Anier, K., Malinovskaja, K., Pruus, K., Aonurm‐Helm, A., Zharkovsky, A., & Kalda, A. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.07.012 · Cited by 82 · see citing works
Zhu, X., Li, T., Peng, S., Ma, X., Chen, X., & Zhang, X. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.005 · Cited by 77 · see citing works
Rees, S. L., Steiner, M. S., & Fleming, A. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.013 · Cited by 71 · see citing works
Ventura, R., Coccurello, R., Andolina, D., Latagliata, E. C., Zanettini, C., Lampis, V., Battaglia, M., D'Amato, F. R., & Moles, A. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs145 · Cited by 68 · see citing works
Horii‐Hayashi, N., Sasagawa, T., Matsunaga, W., Matsusue, Y., Azuma, C., & Nishi, M. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02377.x · Cited by 55 · see citing works
Self-citationEarly life stress induces renal dysfunction in adult male rats but not female rats
Loria, A. S., Yamamoto, T., Pollock, D. M., & Pollock, J. S. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00364.2012 · Cited by 38 · see citing works
Hedonic sensitivity to natural rewards is affected by prenatal stress in a sex-dependent manner
Reynaert, M., Marrocco, J., Mairesse, J., Lionetto, L., Simmaco, M., Deruyter, L., Allorge, D., Moles, A., Pittaluga, A., Maccari, S., et al. (2015) · Addiction Biology · doi:10.1111/adb.12270 · Cited by 37 · see citing works
Orendain-Jaime, E. N., Ortega‐Ibarra, J., & López‐Pérez, S. J. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.09.001 · Cited by 33 · see citing works
Todkar, A., Granholm, L., Aljumah, M., Nilsson, K. W., Comasco, E., & Nylander, I. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00090 · Cited by 31 · see citing works
Vrettou, M., Granholm, L., Todkar, A., Nilsson, K. W., Wallén‐Mackenzie, Å., Nylander, I., & Comasco, E. (2015) · Addiction Biology · doi:10.1111/adb.12331 · Cited by 24 · see citing works
Sex differences in dopamine binding and modafinil conditioned place preference in mice
Bernardi, R. E., Broccoli, L., Spanagel, R., & Hansson, A. C. (2015) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2015.08.016 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The effects of early life stress on reward processing
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.002 · Cited by 192 · see citing works
“, 1996b, 1996a) as well as decreased conditioned place preference to chocolate (Sasagawa et al., 2017) indicative of a decreased reward valuation/incentive salience function within the approach motivation construct.”
BackgroundMechanisms linking childhood adversity with psychopathology: Learning as an intervention target
McLaughlin, K. A., DeCross, S. N., Jovanović, T., & Tottenham, N. (2019) · Behaviour Research and Therapy · doi:10.1016/j.brat.2019.04.008 · Cited by 198 · see citing works
Nishi, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197212 · Cited by 146 · see citing works
Self-citationImpact of Early Life Stress on Reward Circuit Function and Regulation
Hanson, J. L., Williams, A. V., Bangasser, D. A., & Peña, C. J. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.744690 · Cited by 123 · see citing works
Epigenetics of childhood trauma: Long term sequelae and potential for treatment
Thumfart, K. M., Jawaid, A., Bright, K., Flachsmann, M., & Mansuy, I. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.042 · Cited by 78 · see citing works
Dopamine Circuit Mechanisms of Addiction-Like Behaviors
Poisson, C. L., Engel, L., & Saunders, B. T. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.752420 · Cited by 75 · see citing works
Adverse effects of early-life stress: focus on the rodent neuroendocrine system
Lee, S. H., & Jung, E. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.377587 · Cited by 43 · see citing works
Bonapersona, V., Joëls, M., & Sarabdjitsingh, R. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.003 · Cited by 42 · see citing works
Social defeat stress: Mechanisms underlying the increase in rewarding effects of drugs of abuse
Montagud‐Romero, S., Blanco-Gandía, M. C., Reguilón, M. D., Perez, C. F., Ballestín, R., Miñarro, J., & Rodríguez‐Arias, M. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14127 · Cited by 40 · see citing works
The epigenetics of animal personality
van Oers, K., van den Heuvel, K., & Sepers, B. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105194 · Cited by 40 · see citing works
Epigenetic Mechanism of Early Life Stress-Induced Depression: Focus on the Neurotransmitter Systems
Cheng, Z., Su, J., Zhang, K. N., Jiang, H., & Li, B. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.929732 · Cited by 41 · see citing works
The effects of early life stress on motivated behaviors: A role for gonadal hormones
Eck, S. R., & Bangasser, D. A. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.014 · Cited by 38 · see citing works
The effects of early life stress on impulsivity
Sanchez, E. O., & Bangasser, D. A. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104638 · Cited by 40 · see citing works
Evolutionary Consequences of Social Isolation
Bailey, N. W., & Moore, A. J. (2018) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2018.05.008 · Cited by 36 · see citing works
The Epigenetics of Early Life Adversity: Current Limitations and Possible Solutions
Barnett-Burns, S., Almeida, D. M., & Turecki, G. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.01.008 · Cited by 34 · see citing works
Taff, C. C., Campagna, L., & Vitousek, M. N. (2019) · Molecular Ecology · doi:10.1111/mec.15186 · Cited by 35 · see citing works
Epigenetic regulation of neurotransmitter signaling in neurological disorders
Wu, T., Cai, W., & Chen, X. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106232 · Cited by 33 · see citing works
Louwies, T., & Meerveld, B. G. (2019) · Neurogastroenterology & Motility · doi:10.1111/nmo.13751 · Cited by 33 · see citing works
Zhang, X., Xun, Y., Wang, L., Zhang, J., Hou, W., Ma, H., Cai, W., Li, L., Guo, Q., Li, Y., et al. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147497 · Cited by 33 · see citing works
Translational models of stress and resilience: An applied neuroscience methodology review
Albayrak, Z. S., Vaz, A., Bordes, J., Ünlü, S., Sep, M. S. C., Vinkers, C. H., Pinto, L., & Eser, H. Y. (2024) · Neuroscience Applied · doi:10.1016/j.nsa.2024.104064 · Cited by 39 · see citing works
Agrawal, P., Chung, P., Heberlein, U., & Kent, C. F. (2019) · BMC Biology · doi:10.1186/s12915-019-0646-4 · Cited by 29 · see citing works
Blair, K. S., Aloi, J. M., Bashford‐Largo, J., Zhang, R., Elowsky, J., Lukoff, J., Vogel, S., Carollo, E., Schwartz, A., Pope, K., et al. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.101051 · Cited by 31 · see citing works
Endo, N., Makinodan, M., Mannari‐Sasagawa, T., Horii‐Hayashi, N., Somayama, N., Komori, T., Kishimoto, T., & Nishi, M. (2021) · Scientific Reports · doi:10.1038/s41598-020-80206-3 · Cited by 30 · see citing works
Self-citationOswald, L. M., Dunn, K. E., Seminowicz, D. A., & Storr, C. L. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11040315 · Cited by 28 · see citing works
Köhler, J. C., Gröger, N., Lesse, A., Guara Ciurana, S., Rether, K., Fegert, J., Bock, J., & Braun, K. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1199-1 · Cited by 28 · see citing works
Christensen, M. C., Florea, I., Loft, H., & McIntyre, R. S. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.11.074 · Cited by 26 · see citing works
Duque-Quintero, M., Hooijmans, C. R., Hurowitz, A., Ahmed, A., Barris, B., Homberg, J. R., Hen, R., Harris, A. Z., Balsam, P. D., & Atsak, P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104849 · Cited by 24 · see citing works
Santos‐Toscano, R., Arévalo, M., García‐Segura, L. M., Grassi, D., & Lagunas, N. (2023) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2023.101085 · Cited by 22 · see citing works
A role for adaptive developmental plasticity in learning and decision making
Lin, W. C., Delevich, K. M., & Wilbrecht, L. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.07.010 · Cited by 24 · see citing works
Demaili, A., Portugalov, A., Dudai, M., Maroun, M., Akirav, I., Braun, K., & Bock, J. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1129946 · Cited by 23 · see citing works
Emerging role of microglia in the developing dopaminergic system: Perturbation by early life stress
She, K., Yuan, N., Huang, M., Zhu, W., Tang, M., Ma, Q., & Chen, J. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00742 · Cited by 20 · see citing works
Emmons, R., Sadok, T., Rovero, N. G., Belnap, M. A., Henderson, H. J. M., Quan, A., Toro, N. J. D., & Halladay, L. R. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24644 · Cited by 19 · see citing works
Vester, A. I., Hermetz, K. E., Burt, A., Everson, T. M., Marsit, C. J., & Caudle, W. M. (2020) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2020.106887 · Cited by 19 · see citing works
Early adversity and the regulation of gene expression: implications for prenatal health
Gillespie, S. L., Cole, S. W., & Christian, L. M. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.02.005 · Cited by 17 · see citing works
vonHoldt, B. M., Kartzinel, R. Y., van Oers, K., Verhoeven, K. J. F., & Ouyang, J. Q. (2022) · Journal of Animal Ecology · doi:10.1111/1365-2656.13878 · Cited by 16 · see citing works
A Painful Beginning: Early Life Surgery Produces Long-Term Behavioral Disruption in the Rat
Ririe, D. G., Eisenach, J. C., & Martin, T. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.630889 · Cited by 16 · see citing works
Environmental Contributions to Anhedonia
Harkness, K. L., Lamontagne, S. J., & Cunningham, S. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_289 · Cited by 17 · see citing works
Early life adversity across different cell- types in the brain
Warhaftig, G., Almeida, D. M., & Turecki, G. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105113 · Cited by 16 · see citing works
Chronic central oxytocin infusion impairs sociability in mandarin voles
Du, P., He, Z., Cai, Z., Hao, X., Dong, N., Yuan, W., Hou, W., Yang, J., Jia, R., & Tai, F. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.09.006 · Cited by 14 · see citing works
Ruigrok, S. R., Kotah, J. M., Kuindersma, J. E., Speijer, E., van Irsen, A. A. S., la Fleur, S. E., & Kőrösi, A. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100360 · Cited by 15 · see citing works
Soares, J. A. G., Sutley-Koury, S. N., Pomrenze, M. B., & Tucciarone, J. (2025) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2024.1521016 · Cited by 13 · see citing works
Adverse childhood experience and depression: the role of gut microbiota
Bai, Y., Shu, C., Hou, Y., & Wang, G. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1309022 · Cited by 13 · see citing works
Rivi, V., Rigillo, G., Toscano, Y., Benatti, C., & Blom, J. M. C. (2023) · Children · doi:10.3390/children10071217 · Cited by 12 · see citing works
Xu, X. F., Chen, J., Long, L. H., Zhang, A. M., Yang, J., Li, Y. J., Chen, L., Zhong, X. L., Xu, Y., & Cao, W. Y. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.08.173 · Cited by 10 · see citing works
McNeal, N., Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., Dagner, A., Ihm, E., Wardwell, J., & Grippo, A. J. (2019) · Autonomic Neuroscience · doi:10.1016/j.autneu.2019.03.003 · Cited by 8 · see citing works
Effect of prenatal transportation stress on DNA methylation in Brahman heifers
Baker, E. C., Cilkiz, K. Z., Riggs, P. K., Littlejohn, B. P., Long, C. R., Welsh, T. H., Randel, R. D., & Riley, D. G. (2020) · Livestock Science · doi:10.1016/j.livsci.2020.104116 · Cited by 8 · see citing works
Is Adolescence a Sensitive Period for the Development of Incentive-Reward Motivation?
Luciana, M., & Collins, P. F. (2021) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2021_275 · Cited by 7 · see citing works
Henderson, H. J. M., Etem, G., Bjorni, M., Belnap, M. A., Rosellini, B., & Halladay, L. R. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113241 · Cited by 7 · see citing works
How dopamine guides our social world
Padilla-Coreano, N., & Martínez-Rivera, F. J. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100085 · Cited by 6 · see citing works
Wallace, K. J., Dupeyron, S., Li, M., & Kelly, A. M. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06513-5 · Cited by 5 · see citing works
Eslami, A., Moghaddam, A. H., Jelodar, S. K., & Ranjbar, M. (2025) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2025.03.004 · Cited by 4 · see citing works
Bertollo, A. G., Puntel, C. F., Rievers, H. F. B., Brunhara, E. G. S., & Ignácio, Z. M. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.01.008 · Cited by 4 · see citing works
Interactions of sex and stress in modulation of ventral tegmental area dopaminergic activity
Price, K. M., & Polter, A. M. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101477 · Cited by 4 · see citing works
Early Life Stress and DNA Methylation
Mundorf, A., & Freund, N. (2019) · RNA technologies · doi:10.1007/978-3-030-14792-1_9 · Cited by 4 · see citing works
Life-course effects of early life adversity exposure on eating behavior and metabolism
de Lima, R. M. S., Barth, B., Arcego, D. M., Krolow, R., Silveira, P. P., & Dalmaz, C. (2021) · Advances in food and nutrition research · doi:10.1016/bs.afnr.2021.02.003 · Cited by 4 · see citing works
Environmental Influence on Epigenetics
Resendiz, M., Watkins, D. S., Öztürk, N. C., & Zhou, F. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-91909-8.00036-0 · Cited by 4 · see citing works
Anderson, L. G., Tischer, A. E., Bock, R., Michaelides, M., & Alvarez, V. A. (2026) · Translational Psychiatry · doi:10.1038/s41398-026-04033-2 · Cited by 3 · see citing works
Lonstein, J. S., Vitale, E. M., Olekanma, D. I., McLocklin, A., Pence, N., Bredewold, R., Veenema, A. H., Johnson, A. W., & Burt, S. A. (2023) · Developmental Psychobiology · doi:10.1002/dev.22421 · Cited by 4 · see citing works
Neural mechanisms underlying sex differences in anxiety and depressive disorders
Wei, L., & Li, K. (2024) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/tb-2024-0386 · Cited by 3 · see citing works
Kin, K., Gaini, R., & Niwa, M. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819641-0.00090-6 · Cited by 3 · see citing works
Nguyen, J. H. G., Shimizu, K., Zlotnik, V., Nguyen, M. N., Toro, S. D., Nguyen, M. T., Ronquillo, J., & Halladay, L. R. (2025) · PLoS ONE · doi:10.1371/journal.pone.0331457 · Cited by 2 · see citing works
vonHoldt, B. M., Kartzinel, R. Y., van Oers, K., Verhoeven, K. J. F., & Ouyang, J. Q. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.04.442647 · Cited by 2 · see citing works
An, L., Xiong, Y., Yang, Y., Lyu, D., Yang, Z. R., & Zhang, T. (2025) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2025.173981 · Cited by 1 · see citing works
Effect of early-life stress on LINE-1 in animal model of child neglect
Okano, M., Ogata, A., Aboshi, H., & Kondo, M. (2025) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2025.151787 · Cited by 1 · see citing works
Nguyen, J., Shimizu, K., Zlotnik, V., Nguyen, M. N., Toro, S. D., Nguyen, M., Ronquillo, J., & Halladay, L. R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.08.647890 · Cited by 1 · see citing works
Murgeitio, S., & Andrés, C. (2020)
Dory, E. K., Hazani, R., Loterstein, Y., Zalsman, G., Michal Lavidor, B., & Weller, A. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111511
Epigenetic regulation of inflammation by dopamine in primary human macrophages
Agarwal, Y., Ramani, M. D., Manikandan, S., Bonar, K. A., Montilla, J., Gaskill, P. J., & Matt, S. M. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1779072
- Authors
- Sasagawa, T., Horii-Hayashi, N., Okuda, A., Hashimoto, T., Azuma, C., & Nishi, M.
- Affiliations
- Nara Medical University (JP)
- University of Fukui (JP)
- Corresponding author
- Nishi, Mayumi
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 641
- Pages
- 33-39
- ISSN
- 0304-3940 (ISSN-L)
- OpenAlex
- W2572593764
- Cited by
- 68
- References
- 32
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 6 · 2023: 9 · 2022: 5 · 2021: 15 · 2020: 7 · 2019: 8 · 2018: 6 · 2017: 1
- FWCI
- 2.94
- Type
- journal article
- Language
- en
- Open access
- green
- ginmu.repo.nii.ac.jp
- Licence
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc-nd)
- Nara Medical University Institutional Repository (GINMU) (Nara Medical University) (submittedVersion)
- Funders
- Japan Society for the Promotion of Science (26 7097, JP23390040)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- maternal separation, social isolation, early life stress, reward seeking, dopamine D1 receptor, nucleus accumbens, DNA methylation, epigenetic regulation, tyrosine hydroxylase, ventral tegmental area, sex differences, conditioned place preference, palatable food, child abuse
- MeSH terms
- Animals, Female, Male, Maternal Deprivation, Mice, Inbred C57BL, Nucleus Accumbens, Promoter Regions, Genetic, Reward, Sex Factors, Social Isolation, Receptors, Dopamine D1, DNA Methylation
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
