The DOI matches its Crossref record; 96 of the 96 references it cites were found in a registry or an index.
Variations in Nucleus Accumbens Dopamine Associated with Individual Differences in Maternal Behavior in the Rat
Open accessAbstract
Lactating rats exhibit stable individual differences in pup licking/grooming. We used in vivo voltammetry to monitor changes in extracellular dopamine (DA) in the nucleus accumbens (n. Acc) shell of lactating rats interacting with pups and found that (1) the DA signal increased significantly with pup licking/grooming; (2) the onset of such increases preceded pup licking/grooming; and (3) the magnitude and duration of the increase in the DA signal were significantly correlated with the duration of the licking/grooming bout. In females characterized on the basis of behavioral observations as high-licking/grooming mothers, the magnitude of the increase in the DA signal associated with licking/grooming was significantly greater than in low-licking/grooming dams. Dopamine transporter binding in the n. Acc was increased in low-compared with high-licking/grooming mothers. Injection of the selective DA uptake inhibitor GBR 12909 [1-(2-(Bis-(4-fluorophenyl)methoxy)ethyl)-4-(3 phenypropyl)piperazine dihydrochloride] (5 mg/kg, s.c.) increased the DA signal in the n. Acc and pup licking/grooming in low-licking/grooming mothers to levels comparable with those observed in high-licking/grooming dams. Receptor autoradiographic studies showed elevated levels of D 1 and D 3 receptors in the n. Acc shell region in high-licking/grooming dams. These results suggest that high- and low-licking/grooming dams differ in mesolimbic dopaminergic activity associated with mother-pup interactions. Such differences may serve as neural substrates for individual differences in the motivational component of maternal behavior.
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“Studies on rodent models and neuroimaging studies have shown that activation of the attachment system underpinning both caregiving and partner preference is associated with the activation of two specific systems that have consistently been shown to play an important role in promoting and maintaining maternal behavior: (a) the dopaminergic reward processing system (Champagne et al., 2004; Strathe”
From A developmental, mentalization-based approach to the understanding and treatment of borderline personality disorder (2009) · cites this paper as Champagne et al., 2004
Experimental — accuracy not yet measuredIn the citing paper
“Non-human primate studies have shown that the firing rate of dopaminergic neurons is increased in response to “positive prediction errors”, meaning unexpected natural or conditioned rewards (56).”
From What’s in a smile? Maternal brain responses to infant facial cues (2008) · cites this paper as [56]
In the citing paper
“Although functional MRI only measures blood-oxygen level dependent changes in brain activity, together these studies suggest that positive sensory cues from infants, such as a smiling facial expression, may stimulate dopamine release in the striatum, and promote responsive maternal care.”
From What’s in a smile? Maternal brain responses to infant facial cues (2008) · cites this paper as [56]
In the citing paper
“Maternal rats exhibiting high levels of pup licking and grooming behavior tend to exhibit larger increases in dopaminergic activity in the nucleus accumbens as a result of grooming their pups relative to their low licking and grooming counterparts (Shahrokh et al., 2010, Champagne et al., 2004).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Champagne et al., 2004
In the citing paper
“Dopamine is released within the nucleus accumbens when a mother rat grooms or licks her offspring or after being reunited with her offspring after forced separation (Champagne et al., 2004, Hansen et al., 1993).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Champagne et al., 2004
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Cites
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AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
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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
Self-citationNongenomic 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
Self-citationIkemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450
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
Self-citationMaternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195
Self-citationNeurobehavioural mechanisms of reward and motivation
Robbins, T. W., & Everitt, B. J. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80077-8 · Cited by 1,187
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
Modulation of neurotransmitter release by presynaptic autoreceptors
Starke, K., Göthert, M., & Kilbinger, H. J. (1989) · Physiological Reviews · doi:10.1152/physrev.1989.69.3.864 · Cited by 927
Research works printed but not linked: 9
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Epigenetics and the biological definition of gene×environment interactions
Meaney, M. J. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01381.x · Cited by 1,239
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Dopamine: Functions, Signaling, and Association with Neurological Diseases
Klein, M. O., Battagello, D. S., Cardoso, A. R., Hauser, D. N., Bittencourt, J. C., & Correa, R. G. (2019) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-018-0632-3 · Cited by 1,073
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Metadata
- Authors
- Champagne, F. A., Chretien, P., Stevenson, C. W., Zhang, T. Y., Gratton, A., & Meaney, M. J.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Meaney, Michael J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-04-28
- Volume
- 24
- Issue
- 17
- Pages
- 4113-4123
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6729285
- OpenAlex
- W2114537245
- Cited by
- 398
- References
- 95
- Citations by year
- 2026: 11 · 2025: 11 · 2024: 7 · 2023: 6 · 2022: 13 · 2021: 13 · 2020: 43 · 2019: 14 · 2018: 19 · 2017: 17 · 2016: 18 · 2015: 21 · 2014: 18 · 2013: 23 · 2012: 16
- FWCI
- 19.93
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DMU Open Research Archive (De Montfort University) (submittedVersion)
- Funders
- Canadian Institutes of Health Research
- National Institute of Mental Health (MH060381, R01MH060381)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- maternal behavior, nucleus accumbens shell, dopamine, lactating rats, individual differences, dopamine transporter binding, GBR 12909, dopamine D1 receptor, dopamine D3 receptor, mother-pup interaction
- MeSH terms
- Animals, Animals, Newborn, Behavior, Animal, Binding, Competitive, Dopamine, Electrochemistry, Electrodes, Implanted, Female, Grooming, Individuality, Lactation, Maternal Behavior, Membrane Glycoproteins, Nerve Tissue Proteins, Nucleus Accumbens, Receptors, Dopamine, Time Factors, Tongue, Dopamine Uptake Inhibitors, Rats, Long-Evans, Membrane Transport Proteins, Dopamine Plasma Membrane Transport Proteins, Rats
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