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

Champagne, Frances A.; Chretien, P; Stevenson, Carl W.; Zhang, Tie Yuan; Gratton, Alain; Meaney, Michael J.

doi:10.1523/jneurosci.5322-03.2004

Cited by 328 publications

(280 citation statements)

References 94 publications

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“…The postpartum female is uniquely and highly responsive to pups: she vigorously performs maternal caregiving behaviors toward her pups across the postpartum period and attributes considerable incentive salience to pups during early postpartum (Wilsoncroft 1969;Lee et al 2000;Mattson et al 2001). Pup-directed maternal behaviors substantially increase dopaminergic activity in the nucleus accumbens (Hansen et al 1993;Champagne et al 2004), a mesolimbic region closely tied to motivational processing, goal-directed behaviors (Berridge and Robinson 1998;Ikemoto and Panksepp 1999;Salamone and Correa 2002), and, recently, cocaine-associated chamber preference (Mattson and Morrell 2005). As dynamic endogenous changes in the female's endocrine state also modulate mesolimbic responsivity (Bazzett and Becker 1994;Bakowska and Morrell 1995), both pup-induced and endocrineassociated changes in dopaminergic tone across postpartum may contribute to cocaine's unique incentive salience in the postpartum female rat.…”

Section: Discussionmentioning

confidence: 99%

Incentive salience of cocaine across the postpartum period of the female rat

et al. 2008

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Rationale-Objectives-Our prior conditioned place preference (CPP) work demonstrates that late (day16) postpartum female rats consistently prefer cocaine-over pup-associated chambers, whereas far fewer early postpartum (day8) females prefer the cocaine-associated chamber. The present study examines early and late postpartum females' preference for a cocaine-associated chamber when contrasted with a chamber associated with saline (rather than pups).Materials and methods-Postpartum females were tested for conditioned preference for chambers associated with cocaine (10 mg/kg subcutaneous (SC) or 0.5, 5, 10, or 20 mg/kg intraperitoneal (IP) injections) versus saline; preferences of virgin female and male rats for select cocaine stimuli (10mg/kg SC or IP) were also tested. Locomotion was recorded during CPP conditioning and testing.Results-Early and late postpartum females expressed strikingly similar preference for the cocaineassociated chamber across all administration routes and doses. IP cocaine produced an orderly, inverted U-shaped dose-preference curve, with preference peaking at the 5 mg/kg dose (83% of females). While many postpartum females preferred 10mg/kg cocaine administered either SC or IP, both virgin females and males expressed strong aversion to SC cocaine and, while virgin females strongly preferred IP cocaine, males remained relatively indifferent. Across 10mg/kg IP cocaineconditioning sessions, locomotor sensitization occurred exclusively in cocaine-but not salinepreferring postpartum females. Locomotor rate was lower in preferred versus nonpreferred chambers at CPP test.Conclusions-Early and late postpartum females may be equally and uniquely susceptible to sampling and/or abuse of modestly salient doses of cocaine (10mg/kg SC; 5mg/kg IP) compared to virgin females and/or males.

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Section: Discussionmentioning

confidence: 99%

Incentive salience of cocaine across the postpartum period of the female rat

et al. 2008

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“…Consequently, central infusion of a selective OTR antagonist results in a reduction in LG in High LG lactating dams with negligible effects in Low LG dams [51]. In addition to these hypothalamic systems, there is evidence for the role of mesolimbic dopamine activity in the expression of LG [45]. Prior to the onset of LG in High LG dams there is a steady increase in the release of dopamine (DA) in the nucleus accumbens (NA).…”

Section: The Neurobiology Of Maternal Licking/groomingmentioning

confidence: 99%

“…Activation of maternal care is thought to involve several nuclei including the bed nucleus of the stria terminalis (BNST), lateral septum (LS), and medial preoptic area ( . In addition to these hypothalamic systems, there is evidence for the role of mesolimbic dopamine activity in the expression of LG [45]. Prior to the onset of LG in High…”

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confidence: 99%

Epigenetic mechanisms and the transgenerational effects of maternal care

Champagne

2008

Frontiers in Neuroendocrinology

686

447

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The transmission of traits across generations has typically been attributed to the inheritance by offspring of genomic information from parental generations. However, recent evidence suggests that epigenetic mechanisms are capable of mediating this type of transmission. In the case of maternal care, there is evidence for the behavioral transmission of postpartum behavior from mothers to female offspring. The neuroendocrine and molecular mediators of this transmission have been explored in rats and implicate estrogen-oxytocin interactions and the differential methylation of hypothalamic estrogen receptors. These maternal effects can influence multiple aspects of neurobiology and behavior of offspring and this particular mode of inheritance is dynamic in response to environmental variation. In this review, evidence for the generational transmission of maternal care and the mechanisms underlying this transmission will be discussed as will the implications of this inheritance system for offspring development and for the transmission of environmental information from parents to offspring. Keywords maternal; epigenetic; DNA methylation; estrogen receptor α; oxytocin; environment; cross-fostering Maternal effects have been demonstrated across many species and serve as an important cue to offspring development. In mammals, the lengthy period of prenatal and postnatal motherinfant interaction provides an opportunity for mothers to influence offspring through a variety of mechanisms. During gestation, interactions between mother and fetus are critical for growth and development and variations in these interactions can have long-term consequences for offspring physiological and psychological health. These effects have best been demonstrated through study of prenatal stress [1] and maternal malnutrition [2;3] in which changes to the mother's neuroendocrine system and physiology produces a shift in fetal neurodevelopment. Likewise, the care received by an infant early in life can produce changes in the development of neural systems regulating response to novelty and social behavior [4]. Thus, the maternal environment experienced by a developing organism can play a critical role in shaping adult patterns of behavior. Moreover, there can be transmission of these effects to subsequent generations through alterations in the reproductive behavior of offspring. Thus maternal care can be transmitted from mothers to daughters and grand-daughters. The mechanisms mediating Correspondence should be addressed to: Dr. Frances A. Champagne, Department of Psychology, Columbia University, Room 406 Schermerhorn Hall, 1190 Amsterdam Avenue, New York, NY 10017, Phone: (212) 854-2589, Fax: (212) 854-3609, Email: E-mail: fac2105@columbia.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is ...

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“…Increased postpartum dopaminergic activity is essential for maternalpup caregiving (Hansen et al, 1991;Stolzenberg and Numan, 2011), with positive correlations between suckling and maternal striatal DA (Champagne et al, 2004). Higher striatal DA concentrations were detected both at 4 days postpartum compared with estrous controls (Glaser et al, 1990) and in parous compared with nulliparous rodents (Byrnes et al, 2001).…”

Section: Introductionmentioning

confidence: 98%

Postpartum and Depression Status are Associated With Lower [11C]raclopride BPND in Reproductive-Age Women

Moses‐Kolko

Price

Wisner

et al. 2012

Neuropsychopharmacol

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The early postpartum period is associated with increased risk for affective and psychotic disorders. Because maternal dopaminergic reward system function is altered with perinatal status, dopaminergic system dysregulation may be an important mechanism of postpartum psychiatric disorders. Subjects included were non-postpartum healthy (n ¼ 13), postpartum healthy (n ¼ 13), nonpostpartum unipolar depressed (n ¼ 10), non-postpartum bipolar depressed (n ¼ 7), postpartum unipolar (n ¼ 13), and postpartum bipolar depressed (n ¼ 7) women. Subjects underwent 60 min of [ 11 C]raclopride-positron emission tomography imaging to determine the nondisplaceable striatal D 2/3 receptor binding potential (BP ND ). Postpartum status and unipolar depression were associated with lower striatal D 2/3 receptor BP ND in the whole striatum (p ¼ 0.05 and p ¼ 0.02, respectively) that reached a maximum of 7-8% in anteroventral striatum for postpartum status (p ¼ 0.02). Unipolar depression showed a nonsignificant trend toward being associated with 5% lower BP ND in dorsal striatum (p ¼ 0.06). D 2/3 receptor BP ND did not differ significantly between unipolar depressed and healthy postpartum women or between bipolar and healthy subjects; however, D 2/3 receptor BP ND was higher in dorsal striatal regions in bipolar relative to unipolar depressives (p ¼ 0.02). In conclusion, lower striatal D 2/3 receptor BP ND in postpartum and unipolar depressed women, primarily in ventral striatum, and higher dorsal striatal D 2/3 receptor BP ND in bipolar relative to unipolar depressives reveal a potential role for the dopamine (DA) system in the physiology of these states. Further studies delineating the mechanisms underlying these differences in D 2/3 receptor BP ND , including study of DA system responsivity to rewarding stimuli, and increasing power to assess unipolar vs bipolarrelated differences, are needed to better understand the affective role of the DA system in postpartum and depressed women.

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

Cited by 328 publications

References 94 publications

Incentive salience of cocaine across the postpartum period of the female rat

Incentive salience of cocaine across the postpartum period of the female rat

Epigenetic mechanisms and the transgenerational effects of maternal care

Postpartum and Depression Status are Associated With Lower [11C]raclopride BPND in Reproductive-Age Women

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