Neurobiology of mother–infant interactions: experience and central nervous system plasticity across development and generations

Fleming, Alison S.; O’Day, Danton H.; Kraemer, Gary W.

doi:10.1016/s0149-7634(99)00011-1

Cited by 384 publications

(274 citation statements)

References 67 publications

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“…A possible role for odor cues has often been found, even in human infants [26,65,84,108,113]. It has been proposed that the dam's manipulations of pups during normal mother/infant interactions may be how rat pups form an attraction to the maternal odor and an attachment to the dam [30]. We suggest that this process underlies the pups' positive response to the sires.…”

Section: Hypothesized Mechanism For Acquisition Of Paternal Potentiationmentioning

confidence: 65%

Acquisition and expression of a socially mediated separation response

Shair¹

2007

Behavioural Brain Research

108

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INTRODUCTIONSocial bonds are made up of numerous subsystems mediating the overall social relationships that develop between infants and caretakers. The effects of an infant's formation of early life relationships and its social interactions with caretakers are known to last well in to adulthood with both beneficial and harmful effects [28,35,70]. In our laboratory, we study the development of social relationships between infant rats and their dams, sires, and littermates using an isolation, reunion, and re-isolation test paradigm.Infant rats emit ultrasonic vocalizations (USV) in a variety of situations, including as a response to isolation, physical manipulation, and thermal and olfactory challenge [1][2][3]6,19,25,46,79,80,82,97]. Many researchers have used the presence and absence of these sounds to make inferences about the internal state of the rodents, e.g., isolation-induced USV's have often been called "distress vocalizations" [29,76,78].The isolation-induced vocalization of a rat pup is modulated both by current social interactions and by the pup's rearing experience. This modulation of USV by social interactions provides a paradigm for investigating the neurobehavioral mechanisms underlying acquisition and expression of infant attachment. What is maternal potentiation of isolation-induced vocalizations of infant rats?Maternal potentiation of ultrasonic vocalization occurs when, after a brief contact with the dam, isolated infant rats produce USV at a rate significantly higher than they would during an isolation not preceded by dam contact. Although the definition may seem of narrow interest, there is a growing belief that the potentiation phenomenon has broad applicability for the study of early life social relationships in many species. But before going further, the reader needs to understand the usual test paradigm in our laboratory.Developmental Psychobiology, Unit 40, New York State Psychiatric Institute, 1051 Riverside Dr. NY, NY 100032, Tele 212-543-5695, Fax 212-543-5467, hns1@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 published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptTest procedure-On the day of testing, the dam is removed from the home cage and anesthetized. The litter is allowed to adapt to her removal for ~15-20min in the home cage on a thermoregulated heating pad. Then, each pup is tested in turn. The pup is picked up and placed alone in a clean polycarbonate rectangular box (18 × 21 × 20 cm) at room temperature. The test consists of three periods, which can range from 1-5min in length (3mi...

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Section: Hypothesized Mechanism For Acquisition Of Paternal Potentiationmentioning

confidence: 65%

Acquisition and expression of a socially mediated separation response

Shair¹

2007

Behavioural Brain Research

108

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mentioning

confidence: 89%

“…Thus, the biological offspring of low LG-ABN mothers reared by high LG-ABN dams resemble the normal offspring of high LG-ABN mothers (and vice versa) (5). These findings suggest that variations in maternal behavior can directly program rudimentary defensive responses to stress and serve as a mechanism for the nongenomic transmission of individual differences in stress reactivity across generations (3,5,12).Previous studies suggest that maternal programming of individual differences in gene expression and stress responses in the rat involves modifications of epigenetic mechanisms, including DNA methylation and histone modification of a nerve growth factorinducible protein A (NGFI-A) transcription factor binding site on a brain-specific GR promoter (13). Increased maternal LG-ABN behavior during the first week of life causes DNA demethylation, increased histone acetylation and NGFI-A binding, and increased hippocampal GR expression (14).…”

mentioning

confidence: 95%

Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood

Weaver

Meaney

Szyf

2006

Proc. Natl. Acad. Sci. U.S.A.

722

504

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Early-life experience has long-term consequences on behavior and stress responsivity of the adult. We previously proposed that early-life experience results in stable epigenetic programming of glucocorticoid receptor gene expression in the hippocampus. The aim of this study was to examine the global effect of early-life experience on the hippocampal transcriptome and the development of stress-mediated behaviors in the offspring and whether such effects were reversible in adulthood. Adult offspring were centrally infused with saline vehicle, the histone deacetylase inhibitor trichostatin A (TSA), or the essential amino acid L-methionine. The animals were assessed in an unfamiliar open-field arena, and the hippocampal transcriptome of each animal was evaluated by microarray analysis. Here we report that TSA and methionine treatment reversed the effect of maternal care on open-field behavior. We identified >900 genes stably regulated by maternal care. A fraction of these differences in gene expression is reversible by either the histone deacetylase inhibitor TSA or the methyl donor L-methionine. These results suggest that early-life experience has a stable and broad effect on the hippocampal transcriptome and anxiety-mediated behavior, which is potentially reversible in adulthood.hypothalamic-pituitary-adrenal stress response ͉ L-methionine ͉ maternal behavior ͉ microarray ͉ trichostatin A I n primates and rodents, as in nonmammalian species, there are maternal effects on defensive responses in the adult offspring (1-3). In the rat, these effects are mediated by variations in maternal care such that maternal behavior stably alters the development of behavioral and endocrine responses to stress in the offspring through tissue-specific effects on gene expression (4, 5). Thus, the adult offspring of mothers that show increased pup licking͞ grooming and arched-back nursing (i.e., high LG-ABN mothers) over the first week of postnatal life exhibit reduced fearfulness and more modest hypothalamic-pituitary-adrenal (HPA) responses to stress.Such maternal effects in the rat target neural systems that tonically inhibit corticotrophin-releasing factor (CRF) synthesis and release in the hypothalamus and amygdala, which serves to activate central noradrenaline in response to stress. Increased noradrenaline, in turn, regulates HPA activity through dynamic regulation of hypothalamic CRF and behavioral responses to stress. Glucocorticoids initiate tonic negative feedback inhibition over CRF synthesis and release and thus dampen HPA responses to stress (6). Glucocorticoid negative feedback is, in part, mediated by glucocorticoid binding to glucocorticoid receptors (GR) in a number of brain regions, including the hippocampus. As adults, the offspring of high LG-ABN mothers show increased hippocampal GR expression and enhanced glucocorticoid feedback sensitivity by comparison to adult animals reared by low LG-ABN mothers (4, 5). Predictably, adult offspring of high LG-ABN mothers show decreased hypothalamic CRF expression and more mo...

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“…There are numerous reports that maternal care can alter offspring behavior (Barron and Riley, 1985, Fleming et al, 1999, Champagne and Meaney, 2001, Huot et al, 2001, Meaney, 2001). There is evidence that experimental perturbation of a litter leads to the whole litter receiving similar disrupted care and that maternal care is driven by the pups and not by the dams making it difficult to control for individual pup-dam interactions (Huot et al, 2001, Marino et al, 2002.…”

Section: Maternal Carementioning

confidence: 99%

Tolerance, opioid-induced allodynia and withdrawal associated allodynia in infant and young rats

Zissen,

Zhang,

McKelvy

et al. 2007

Neuroscience

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Our laboratory has previously characterized age-dependent changes in nociception upon acute morphine withdrawal. This study characterizes changes in mechanical and thermal nociception following acute, intermittent, or continuous morphine administration in infant (postnatal day 5-8) and young (postnatal day 19-21). Morphine was given as a single acute administration (AM), intermittently twice a day for 3 days (IM), or continuously for 72 hours via a subcutaneous pump implanted (CM). AM did not produce long-term changes in mechanical or thermal nociception in either infant or young rats. CM produced changes in mechanical nociception that included the development of tolerance, opioid-induced mechanical allodynia and withdrawal-associated mechanical allodynia in young rats, but only tolerance and a prolonged withdrawal-associated mechanical allodynia in infant rats. IM produced withdrawal-associated mechanical allodynia in both infant and young rats. Measuring paw withdrawal responses to thermal stimuli, infant and young rats showed tolerance without opioid-induced thermal hyperalgesia or withdrawal-associated thermal hyperalgesia following CM. In contrast to CM, withdrawal-associated thermal hyperalgesia was seen in both ages following IM. In conclusion, CM versus IM differentially modified mechanical and thermal nociception, suggesting that opioid-dependent thermal hyperalgesia and mechanical allodynia can be dissociated from each other in infant and young rats. Furthermore, tolerance, opioidinduced hypersensitivity, and withdrawal-associated hypersensitivity are age-specific and may be mediated by distinct mechanisms.Keywords morphine withdrawal; spinal cord; allodynia; hyperalgesia; neonatal rat It has long been recognized that morphine exerts two paradoxical actions on the adult nervous system: the inhibition of pain processing manifested as analgesia and the facilitation of nociceptive sensitivity manifested as allodynia and hyperalgesia (Bederson et al., 1990, Kim et al., 1990, Kaplan and Fields, 1991. This facilitation of nociceptive sensitivity can be observed in as little as 20 min post-morphine administration by precipitating withdrawal with Corresponding Author: Sarah M. Sweitzer, PhD, Department of Pharmacology, Physiology, Neuroscience, University of South Carolina School of Medicine, Columbia, SC 29208, Phone: (803) Fax: (803) 733-1523 Email: sweitzer@med.sc.edu. Section Editor: Dr. Donna Hammond 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 published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access Author ManuscriptNeuroscience. Author manuscript; available in PMC 2008 January 5. (Bede...

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Neurobiology of mother–infant interactions: experience and central nervous system plasticity across development and generations

Cited by 384 publications

References 67 publications

Acquisition and expression of a socially mediated separation response

Acquisition and expression of a socially mediated separation response

Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood

Tolerance, opioid-induced allodynia and withdrawal associated allodynia in infant and young rats

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