Variations in Maternal Care Alter GABAA Receptor Subunit Expression in Brain Regions Associated with Fear

Caldji, Christian; Diorio, Josie; Meaney, Michael J.

doi:10.1038/sj.npp.1300237

Cited by 214 publications

(173 citation statements)

References 60 publications

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“…Maternal licking (and grooming) is one of the most effective actions that the dams can direct toward young offspring [61,62]. This behavior can have dramatic effects on stress hormone levels [61], brain mechanisms related to anxiety [62] and fear reactivity in aversive situations [63].…”

Section: Discussionmentioning

confidence: 99%

Effects of polychlorinated biphenyls on maternal odor conditioning in rat pups

Cromwell

Johnson

McKnight

et al. 2007

Physiology & Behavior

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Polychlorinated biphenyls (PCBs) are pervasive environmental contaminants that can have damaging effects on physiologic, motoric and cognitive function. Results from studies on PCBs and behavior have shown that exposure can alter learning and memory processes and that these shifts in cognitive abilities can be related to changes in hormonal and neural function. Little experimentation has been done on the impact of exposure to PCBs on social and emotional development. Previous work has shown that exposure to PCBs in children can alter play behavior. Importantly, exposure to PCBs has been found to change aspects of maternal-offspring interactions in rodents. The present study examined the impact of PCBs on maternal odor conditioning in rat pups 12-14 days of age. A modified version of the conditioned place preference paradigm was used that incorporated a maternal-associated odor cue (lemon scent) as the conditioned stimulus. PCBs significantly depressed the preference for the maternal-associated cue but did not impair discrimination for a novel odor. These effects could arise due to changes in the social dynamics between the dam and offspring after co-exposure to PCBs. For example, dams exposed to PCBs during gestation have been found to show elevated grooming directed towards pups exposed to PCBs. This change in maternal care can have dramatic effects on behavioral and hormonal systems in the developing rat pup. In conclusion, perinatal PCBs alter important social behaviors of both the mother and pup, and these alterations could have long-lasting effects on behavioral, cognitive and emotional development.

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Section: Discussionmentioning

confidence: 99%

Effects of polychlorinated biphenyls on maternal odor conditioning in rat pups

Cromwell

Johnson

McKnight

et al. 2007

Physiology & Behavior

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“…In addition to these HPA effects, offspring of low LG dams have a decreased density of benzodiazepine receptors in the amygdala compared to the offspring of High LG dams [36; 38;39;40] and GABA subunit expression is altered by maternal LG with implications for benzodiazepine binding [41]. Offspring of Low LG dams also exhibit impaired performance on tests of spatial learning and memory, elevated hippocampal brain derived neurotrophic factor (BDNF) mRNA, and increased hippocampal choline acetyltransferase and synaptophysin [42].…”

Section: Influence Of Maternal Care On Offspring Neurobiology and Behmentioning

confidence: 99%

Epigenetic mechanisms and the transgenerational effects of maternal care

Champagne

2008

Frontiers in Neuroendocrinology

699

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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“…Early life maternal neglect also results in increased levels of α 3 and α 4 in the adult rat amygdala whereas enriched maternal care in the first week of life results in increased α 1 and β 3 mRNA levels almost everywhere, including the hippocampus and amygdala, and increased β 2 and γ 2 in the amygdala. These effects can be reversed by cross-fostering (Caldji et al, 2003).…”

Section: Gaba a Receptors Stress And Ethanolmentioning

confidence: 99%

The role of GABAA receptors in the development of alcoholism

Enoch

2008

Pharmacology Biochemistry and Behavior

197

181

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Alcoholism is a common, heritable, chronic relapsing disorder. GABA A receptors undergo allosteric modulation by ethanol, anesthetics, benzodiazepines and neurosteroids and have been implicated in the acute as well as the chronic effects of ethanol including tolerance, dependence and withdrawal. Medications targeting GABA A receptors ameliorate the symptoms of acute withdrawal. Ethanol induces plasticity in GABA A receptors: tolerance is associated with generally decreased GABA A receptor activation and differentially altered subunit expression. The dopamine (DA) mesolimbic reward pathway originating in the ventral tegmental area (VTA), and interacting stress circuitry play an important role in the development of addiction. VTA GABAergic interneurons are the primary inhibitory regulators of DA neurons and a subset of VTA GABA A receptors may be implicated in the switch from heavy drinking to dependence. GABA A receptors modulate anxiety and response to stress; important elements of sustained drinking and relapse. The GABA A receptor subunit genes clustered on chromosome 4 are highly expressed in the reward pathway. Several recent studies have provided strong evidence that one of these genes, GABRA2, is implicated in alcoholism in humans. The influence of the interaction between ethanol and GABA A receptors in the reward pathway on the development of alcoholism together with genetic and epigenetic vulnerabilities will be explored in this review.

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Variations in Maternal Care Alter GABAA Receptor Subunit Expression in Brain Regions Associated with Fear

Cited by 214 publications

References 60 publications

Effects of polychlorinated biphenyls on maternal odor conditioning in rat pups

Effects of polychlorinated biphenyls on maternal odor conditioning in rat pups

Epigenetic mechanisms and the transgenerational effects of maternal care

The role of GABAA receptors in the development of alcoholism

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