Cited by 398Neuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on BehaviorStress Responses and Cortisol

Variations in Nucleus Accumbens Dopamine Associated with Individual Differences in Maternal Behavior in the Rat

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Champagne, Frances A., Chretien, Pablo, Stevenson, Carl W., Zhang, Tie Yuan, Gratton, Alain, Meaney, Michael J.·2004·The Journal of Neuroscience

Abstract

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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Crossref · 10.1523/jneurosci.5322-03.2004

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  • Activation of the attachment system underpinning caregiving and partner preference is associated with activation of the dopaminergic reward processing system and the oxytocinergic system.

    “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

    The paper reports increased nucleus accumbens dopamine during pup licking and grooming in lactating rats (Abstract), supporting the citation’s point about dopaminergic reward processing in caregiving. It does not establish activation of this system during partner preference; its discussion of oxytocin–dopamine interaction is a proposed mechanism for maternal behavior, not evidence for the full attachment-system claim. (LLM, conf=0.84)

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  • Non-human primate studies have shown that firing rate of dopaminergic neurons is increased in response to positive prediction errors.

    “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).”
  • 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.

    “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.”
  • 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.

    “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

  • 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.

    “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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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
Published
2004-04-28
Volume
24
Issue
17
Pages
4113-4123
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
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
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
  • Social Sciences › Psychology › Social Psychology › 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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