Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring
Abstract
Variation within mesolimbic dopamine (DA) pathways has significant implications for behavioral responses to rewards, and previous studies have indicated long-term programming effects of early life stress on these pathways. In the current study, we examined the impact of natural variations in maternal care in Long Evans rats on the development of DA pathways in female offspring and the consequences for reward-directed behaviors. We found that tyrosine hydroxylase (TH) immunoreactivity in the ventral tegmental area was elevated by postnatal day 6 in response to maternal licking/grooming (LG), and that these effects were sustained into adulthood. Increased TH immunoreactivity was not found to be associated with altered epigenetic regulation or transcriptional activation of Th, but probably involved LG-associated changes in the differentiation of postnatal DA neurons through increased expression of Cdkn1c, and enhanced survival of DA projections through LG-associated increases in Lmx1b and brain-derived neurotrophic factor. At weaning, high-LG offspring had elevated DA receptor mRNA levels within the nucleus accumbens and increased conditioned place preference for a high-fat diet. In contrast, high-LG, as compared with low-LG, juvenile offspring had a reduced preference for social interactions with siblings, and haloperidol administration abolished group differences in conditioned place preference through a shift towards increased social preferences in high-LG offspring. The effects of maternal care on developing DA pathways and reward-directed behavior of female offspring that we have observed may play a critical role in the behavioral transmission of maternal LG from mother to daughter, and account for individual differences in the mesolimbic DA system.
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?
In rodent studies, early life adversity (ELA) induces alterations in DA neuronal activity and synaptic function, impacting reward-directed behavior and partially accounting for individual variation along the mesolimbic DA projection.
“In rodent studies, early life adversity (ELA) has been shown to induce alterations in DA neuronal activity and synaptic function [15], impacting reward-directed behavior and partially accounting for individual variation along the mesolimbic DA projection [16].”
From Food Addiction and Psychosocial Adversity: Biological Embedding, Contextual Factors, and Public Health Implications (2020) · cites this paper as [16]
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190 · 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
Self-citationMeaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
The mesolimbic dopamine reward circuit in depression
Nestler, E. J., & Carlezon, W. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.09.018 · Cited by 2,059 · see citing works
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965 · see citing works
Dopamine neuron systems in the brain: An update
Björklund, A., & Dunnett, S. B. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.006 · Cited by 1,777 · see citing works
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Efferent connections of the substantia nigra and ventral tegmental area in the rat
Beckstead, R. M., Domesick, V. B., & Nauta, W. J. H. (1979) · Brain Research · doi:10.1016/0006-8993(79)91001-1 · Cited by 1,293 · 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
Cortico-Basal Ganglia Reward Network: Microcircuitry
Sesack, S. R., & Grace, A. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.93 · Cited by 985 · see citing works
Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking
Stuber, G. D., Sparta, D. R., Stamatakis, A. M., van Leeuwen, W. A., Hardjoprajitno, J. E., Cho, S., Tye, K. M., Kempadoo, K. A., Zhang, F., Deisseroth, K., et al. (2011) · Nature · doi:10.1038/nature10194 · Cited by 878 · 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
Self-citationChampagne, 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
Self-citationDopamine and reward: The anhedonia hypothesis 30 years on
Wise, R. A. (2008) · Neurotoxicity Research · doi:10.1007/bf03033808 · Cited by 580 · see citing works
Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats
Spear, L. P., & Brake, S. C. (1983) · Developmental Psychobiology · doi:10.1002/dev.420160203 · Cited by 539 · see citing works
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · see citing works
Voorn, P., Kalsbeek, A., Jorritsma‐Byham, B., & Groenewegen, H. J. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90041-3 · Cited by 503 · see citing works
Yan, Y., Frisén, J., Lee, M., Massagué, J., & Barbacid, M. (1997) · Genes & Development · doi:10.1101/gad.11.8.973 · Cited by 491 · see citing works
Champagne, F. A., Chretien, P., Stevenson, C. W., Zhang, T. Y., Gratton, A., & Meaney, M. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5322-03.2004 · Cited by 398 · see citing works
Self-citationA second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b
Smidt, M. P., Asbreuk, C. H. J., Cox, J. J., Chen, H., Johnson, R. L., & Burbach, J. P. H. (2000) · Nature Neuroscience · doi:10.1038/73902 · Cited by 394 · see citing works
The pleasures of play: pharmacological insights into social reward mechanisms
Trezza, V., Baarendse, P. J. J., & Vanderschuren, L. J. M. J. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.06.008 · Cited by 372 · see citing works
Glutamatergic neurons are present in the rat ventral tegmental area
Yamaguchi, T., Sheen, W., & Morales, M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05263.x · Cited by 367 · see citing works
Oxytocin–dopamine interactions mediate variations in maternal behavior in the rat
Shahrokh, D. K., Zhang, T.-Y., Diorio, J., Gratton, A., & Meaney, M. J. (2010) · Endocrinology · doi:10.1210/en.2009-1271 · Cited by 366 · see citing works
Smidt, M. P., van Schaick, H. S. A., Lanctôt, C., Tremblay, J., Cox, J. J., van der Kleij, A. A. M., Wolterink, G., Drouin, J., & Burbach, J. P. H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.13305 · Cited by 363 · see citing works
Numan, M., & Stolzenberg, D. S. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.10.002 · Cited by 361 · see citing works
Smidt, M. P., Smits, S. M., Bouwmeester, H., Hamers, F. P. T., van der Linden, A. J. A., Hellemons, A. J. C. G. M., Graw, J., & Burbach, J. P. H. (2004) · Development · doi:10.1242/dev.01022 · Cited by 317 · see citing works
Champagne, F. A., Weaver, I. C. G., Diorio, J. C., Sharma, S., & Meaney, M. J. (2003) · Endocrinology · doi:10.1210/en.2003-0564 · Cited by 295 · see citing works
Self-citationPlace conditioning reveals the rewarding aspect of social interaction in juvenile rats
Calcagnetti, D. J., & Schechter, M. D. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90101-7 · Cited by 284 · see citing works
Maternal Care and DNA Methylation of a Glutamic Acid Decarboxylase 1 Promoter in Rat Hippocampus
Zhang, T., Hellstrom, I. C., Bagot, R. C., Wen, X., Diorio, J. C., & Meaney, M. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1039-10.2010 · Cited by 269 · see citing works
Zhang, M., Balmadrid, C., & Kelley, A. E. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.2.202 · Cited by 268 · see citing works
Hansen, S., Bergvall, Å. H., & Nyiredi, S. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90523-v · Cited by 247 · see citing works
Woolf, N. J., & Butcher, L. L. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90102-2 · Cited by 231 · see citing works
Hansen, S., Harthon, C., Waslin, E., Löfberg, L., & al, E. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.4.588 · Cited by 211 · see citing works
Development of dopaminergic neurons in the mammalian brain
Prakash, N., & Wurst, W. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5387-6 · Cited by 207 · see citing works
Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00418.x · Cited by 198 · see citing works
Comparison of two positive reinforcing stimuli: Pups and cocaine throughout the postpartum period.
Mattson, B. J., Williams, S., Rosenblatt, J. S., & Morrell, J. I. (2001) · Behavioral Neuroscience · doi:10.1037//0735-7044.115.3.683 · Cited by 197 · see citing works
Comparison of two positive reinforcing stimuli: Pups and cocaine throughout the postpartum period.
Mattson, B. J., Williams, S., Rosenblatt, J. S., & Morrell, J. I. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.3.683 · Cited by 197 · see citing works
Decreases in Dietary Preference Produce Increased Emotionality and Risk for Dietary Relapse
Teegarden, S. L., & Bale, T. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.09.032 · Cited by 188 · see citing works
Olson, V. G. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0345-05.2005 · Cited by 186 · see citing works
Hansen, S., Harthon, C., Wallin, E., et al. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.4.588 · Cited by 186 · see citing works
Social play in juvenile rats: A decade of methodological and experimental research
Thor, D. H., & Holloway, W. R. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90004-6 · Cited by 176 · see citing works
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175 · see citing works
Biochemical Adaptations in the Mesolimbic Dopamine System in Response to Repeated Stress
Ortiz, J. (1996) · Neuropsychopharmacology · doi:10.1016/0893-133x(95)00152-4 · Cited by 170 · see citing works
Wallen, K. (1996) · Hormones and Behavior · doi:10.1006/hbeh.1996.0042 · Cited by 169 · see citing works
Cameron, N. M., Corpo, A. D., Diorio, J. C., McAllister, K., Sharma, S., & Meaney, M. J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002210 · Cited by 155 · see citing works
Peña, C. J., Neugut, Y. D., & Champagne, F. A. (2013) · Endocrinology · doi:10.1210/en.2013-1595 · Cited by 150 · see citing works
Self-citationNurr1, an orphan nuclear receptor with essential functions in developing dopamine cells
Perlmann, T., & Wallén‐Mackenzie, Å. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0974-7 · Cited by 149 · see citing works
p57 Kip2 cooperates with Nurr1 in developing dopamine cells
Joseph, B., Wallén‐Mackenzie, Å., Benoit, G., Murata, T., Joodmardi, E., Okret, S., & Perlmann, T. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2635658100 · Cited by 149 · see citing works
Bagot, R. C., Zhang, T.-Y., Wen, X., Nguyen, T. T. T., Nguyen, H.-B., Diorio, J., Wong, T. P., & Meaney, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204599109 · Cited by 141 · see citing works
Seroogy, K. B., Schalling, M., Bren�, S., Dagerlind, �., Chai, S. Y., H�kfelt, T., Persson, H., Brownstein, M. J., Huan, R., Dixon, J. E., et al. (1989) · Experimental Brain Research · doi:10.1007/bf00248288 · Cited by 127 · see citing works
Psychomotor stimulants, social deprivation and play in juvenile rats
Beatty, W. W., Dodge, A. M., Dodge, L. J., White, K., & Panksepp, A. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90445-2 · Cited by 126 · see citing works
Teegarden, S. L., Scott, A., & Bale, T. L. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.05.029 · Cited by 119 · see citing works
Early life protein restriction alters dopamine circuitry
Vucetic, Z., Totoki, K., Schoch, H., Whitaker, K. W., Hill‐Smith, T. E., Lucki, I., & Reyes, T. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.010 · Cited by 119 · see citing works
Gaffori, O., & Le Moal, M. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90373-1 · Cited by 117 · see citing works
Das, S., Grunert, M., Williams, L., & Vincent, S. R. (1997) · Synapse · doi:10.1002/(sici)1098-2396(199703)25:3 · Cited by 103 · see citing works
Stern, J. M., & Taylor, L. A. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00323.x · Cited by 99 · see citing works
Moore, C., & Power, K. L. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250303 · Cited by 98 · see citing works
Potential programming of dopaminergic circuits by early life stress
Rodrigues, A.-J., Leão, P., Carvalho, M., Almeida, O. F. X., & Sousa, N. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2085-3 · Cited by 97 · see citing works
Peartree, N. A., Hood, L. E., Thiel, K. J., Sanabria, F., Pentkowski, N. S., Chandler, K. N., & Neisewander, J. L. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.001 · Cited by 90 · see citing works
Einon, D. F., Humphreys, A. P., Chivers, S. M., Field, S., & Naylor, V. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140407 · Cited by 87 · see citing works
Kostić, V., Gurney, M. E., Deng, H., et al. (1997) · Annals of Neurology · doi:10.1002/ana.410410413 · Cited by 85 · see citing works
Loughlin, S. E., & Fallon, J. H. (1983) · Brain Research · doi:10.1016/0006-8993(83)91029-6 · Cited by 82 · see citing works
Jahng, J. W., Ryu, V., Yoo, S. B., Noh, S. J., Kim, J. Y., & Lee, J. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.063 · Cited by 82 · see citing works
Permanent dopaminergic alterations in the n. accumbens after prenatal stress
Alonso, S. J., Navarro, E., & Rodrı́guez, M. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90433-2 · Cited by 79 · see citing works
Barros, V. G., Berger, M. A., Martijena, I. D., Sarchi, M. I., Pérez, A. A., Molina, V. A., Tarazi, F. I., & Antonelli, M. C. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20119 · Cited by 78 · see citing works
Accumbal dopamine function in postpartum rats that were raised without their mothers
Afonso, V. M., King, S. J., Novakov, M., Burton, C. L., & Fleming, A. S. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.08.016 · 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
Fleming, A. S., Miceli, M. O., & Moretto, D. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90073-2 · Cited by 66 · see citing works
Fleming, A. S. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb28015.x · Cited by 58 · see citing works
Epigenetic, transcriptional and posttranscriptional regulation of the tyrosine hydroxylase gene
Lenartowski, R., & Goc, A. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.07.006 · Cited by 58 · see citing works
Differences in maternal behavior of rats and the sociosexual development of the offspring
Birke, L. I. A., & Sadler, D. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200111 · Cited by 58 · see citing works
Wansaw, M. P., Pereira, M., & Morrell, J. I. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.03.005 · Cited by 57 · see citing works
Jensen Peña, C., & Champagne, F. A. (2013) · Behavioral Neuroscience · doi:10.1037/a0031219 · Cited by 54 · see citing works
Self-citationGoy, R. W., & Wallen, K. (1979) · Psychoneuroendocrinology · doi:10.1016/0306-4530(79)90035-0 · Cited by 54 · see citing works
Rawas, R. E., Klement, S., Kummer, K. K., Fritz, M., Dechant, G., Saria, A., & Zernig, G. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00063 · Cited by 54 · see citing works
He, X., Yi, S., Rhee, Y., Kim, H., Han, Y., Lee, S., Lee, H., Park, C., Lee, Y.-S., Richardson, E., et al. (2011) · Stem Cells · doi:10.1002/stem.739 · Cited by 51 · see citing works
The effect of selective D1 and D2 dopaminergic agents on sexual receptivity in the female rat
Grierson, J. P., James, M. D., Pearson, J. R., & Wilson, C. A. (1988) · Neuropharmacology · doi:10.1016/0028-3908(88)90169-4 · Cited by 49 · see citing works
Post‐transcriptional Regulation of Tyrosine Hydroxylase Expression in Adrenal Medulla and Brain
Tank, A. W., Lu, X., Chen, X. M., Radcliffe, P. M., & Sterling, C. R. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1410.054 · Cited by 49 · see citing works
Hu, X., Koeltzow, T. E., Cooper, D., Robertson, G. S., White, F. J., & Vezina, P. (2002) · Synapse · doi:10.1002/syn.10095 · Cited by 44 · see citing works
Maternal care associates with play dominance rank among adult female rats
Parent, C. I., Corpo, A. D., Cameron, N. M., & Meaney, M. J. (2012) · Developmental Psychobiology · doi:10.1002/dev.21070 · Cited by 43 · see citing works
Baker, R. W., Osman, J. L., & Bodnar, R. J. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00528-7 · Cited by 30 · see citing works
Effects of a new postnatal stress model on monoaminergic neurotransmitters in rat brains
Huppertz-Kessler, C. J., Poeschl, J., Hertel, R., Unsicker, K., & Schenkel, J. (2011) · Brain and Development · doi:10.1016/j.braindev.2011.07.008 · Cited by 28 · see citing works
Variation in Maternal Care Influences Ventromedial Hypothalamus Activation in the Rat
Cameron, N. M., Soehngen, E. P., & Meaney, M. J. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02124.x · Cited by 26 · see citing works
Liang, J., Ma, S.-S., Li, Y.-J., Ping, X., Hu, L., & Cui, C. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0739-8 · Cited by 24 · see citing works
Shim, I., Won, J., Lee, J.-K., Song, D.-K., Kim, S. E., Huh, S., Kim, Y.-H., & Suh, H. (2000) · Journal of Ethnopharmacology · doi:10.1016/s0378-8741(99)00166-x · Cited by 18 · see citing works
Efferent connexions of the pars lateralis of the substantia nigra (SNL).
Kaelber, W. W., & Afifi, A. K. (1979) · PubMed · Cited by 11 · see citing works
Compensatory social responses of older pigtailed monkeys to maternal separation
Bernstein, I. S., & Dobrofsky, M. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140210 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Early life stress and development: potential mechanisms for adverse outcomes
Smith, K. E., & Pollak, S. D. (2020) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-020-09337-y · Cited by 500 · see citing works
The biology of mammalian parenting and its effect on offspring social development
Rilling, J. K., & Young, L. J. (2014) · Science · doi:10.1126/science.1252723 · Cited by 452 · see citing works
Atzil, S., Gao, W., Fradkin, I., & Barrett, L. F. (2018) · Nature Human Behaviour · doi:10.1038/s41562-018-0384-6 · Cited by 415 · see citing works
Moustafa, A. A., Parkes, D., Fitzgerald, L., Underhill, D., Garami, J., Levy-Gigi, E., Stramecki, F., Valikhani, A., Frydecka, D., & Misiak, B. (2021) · Current Psychology · doi:10.1007/s12144-018-9973-9 · Cited by 128 · see citing works
Early adverse experience and substance addiction: Dopamine, oxytocin, and glucocorticoid pathways
Kim, S., Kwok, S., Mayes, L. C., Potenza, M. N., Rutherford, H. J. V., & Strathearn, L. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13140 · Cited by 85 · see citing works
Wiss, D. A., Avena, N., & Gold, M. (2020) · Nutrients · doi:10.3390/nu12113521 · Cited by 66 · see citing works
- Authors
- Peña, C. J., Neugut, Y. D., Calarco, C. A., & Champagne, F. A.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Columbia University (US)
- Yale University (US)
- Corresponding author
- Champagne, Frances A.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2014-01-21
- Volume
- 39
- Issue
- 6
- Pages
- 946-956
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2120962478
- Cited by
- 120
- References
- 89
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 2 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 24 · 2019: 13 · 2018: 12 · 2017: 8 · 2016: 11 · 2015: 17 · 2014: 6
- FWCI
- 6.40
- Type
- journal article
- Language
- en
- Update notices
- correction (2021-12-21)
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NIH Office of the Director (1DP2OD001674-01)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal care, mesolimbic dopamine system, ventral tegmental area, tyrosine hydroxylase, CDKN1C, Lmx1b, brain-derived neurotrophic factor, dopamine receptor expression, nucleus accumbens, conditioned place preference, high-fat diet, social behavior, haloperidol, epigenetic regulation, Long-Evans rats, female offspring, early life stress, intergenerational transmission
- MeSH terms
- Animals, Female, Maternal Behavior, Mesencephalon, Receptors, Dopamine, Reward, RNA, Messenger, Transcription Factors, Tyrosine 3-Monooxygenase, Brain-Derived Neurotrophic Factor, Rats, Long-Evans, Cyclin-Dependent Kinase Inhibitor p21, Rats, Dopaminergic Neurons, LIM-Homeodomain Proteins
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
