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      Natural variation in early parental care correlates with social behaviors in adolescent prairie voles ( Microtus ochrogaster)

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          Abstract

          Natural variation in early parental care may contribute to long-term changes in behavior in the offspring. Here we investigate the role of variable early care in biparental prairie voles ( Microtus ochrogaster). Total amounts of parental care were initially quantified for 24 breeder pairs and pairs were ranked in relation to one another based on total contact. Consistency in key components of care suggested a trait-like quality to parental care. Based on this ranking, breeder pairs from the top (high-contact) and bottom (low-contact) quartiles were selected to produce high- and low-contact offspring to investigate adolescent behavior after varying early care. Parental care of subject offspring was again observed postnatally. Offspring of high-contact parents spent more time passively nursing and received more paternal non-huddling contact while low-contact offspring spent more time actively nursing and received more paternal huddling and pseudohuddling in the first postnatal days (PNDs). Low-contact offspring also displayed faster rates of development on a number of physical markers. Post-weaning, offspring were evaluated on anxiety-like behavior, social behavior and pre-pulse inhibition (PPI) to a tactile and an acoustic startle. High-contact offspring spent more time sniffing a juvenile and less time autogrooming. With an infant, high-contact offspring spent more time in non-huddling contact and less time autogrooming and retrieving than did low-contact offspring. Considering sexes separately, high-contact females spent more time sniffing a novel juvenile than low-contact females. High-contact males spent more time in non-huddling contact with an infant than low-contact males; while low-contact females retrieved infants more than high-contact females. In both measures of social behavior, high-contact males spent less time autogrooming than low-contact males. These results suggest a relationship between early-life care and differences in social behavior in adolescence.

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          Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress.

          Variations in maternal care affect the development of individual differences in neuroendocrine responses to stress in rats. As adults, the offspring of mothers that exhibited more licking and grooming of pups during the first 10 days of life showed reduced plasma adrenocorticotropic hormone and corticosterone responses to acute stress, increased hippocampal glucocorticoid receptor messenger RNA expression, enhanced glucocorticoid feedback sensitivity, and decreased levels of hypothalamic corticotropin-releasing hormone messenger RNA. Each measure was significantly correlated with the frequency of maternal licking and grooming (all r's > -0.6). These findings suggest that maternal behavior serves to "program" hypothalamic-pituitary-adrenal responses to stress in the offspring.
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            Nongenomic transmission across generations of maternal behavior and stress responses in the rat.

            In the rat, variations in maternal care appear to influence the development of behavioral and endocrine responses to stress in the offspring. The results of cross-fostering studies reported here provide evidence for (i) a causal relationship between maternal behavior and stress reactivity in the offspring and (ii) the transmission of such individual differences in maternal behavior from one generation of females to the next. Moreover, an environmental manipulation imposed during early development that alters maternal behavior can then affect the pattern of transmission in subsequent generations. Taken together, these findings indicate that variations in maternal care can serve as the basis for a nongenomic behavioral transmission of individual differences in stress reactivity across generations.
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              Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat.

              The mothers of infant rats show individual differences in the frequency of licking/grooming and arched-back nursing (LG-ABN) of pups that contribute to the development of individual differences in behavioral responses to stress. As adults, the offspring of mothers that exhibited high levels of LG-ABN showed substantially reduced behavioral fearfulness in response to novelty compared with the offspring of low LG-ABN mothers. In addition, the adult offspring of the high LG-ABN mothers showed significantly (i) increased central benzodiazepine receptor density in the central, lateral, and basolateral nuclei of the amygdala as well as in the locus ceruleus, (ii) increased alpha2 adrenoreceptor density in the locus ceruleus, and (iii) decreased corticotropin-releasing hormone (CRH) receptor density in the locus ceruleus. The expression of fear and anxiety is regulated by a neural circuitry that includes the activation of ascending noradrenergic projections from the locus ceruleus to the forebrain structures. Considering the importance of the amygdala, notably the anxiogenic influence of CRH projections from the amygdala to the locus ceruleus, as well as the anxiolytic actions of benzodiazepines, for the expression of behavioral responses to stress, these findings suggest that maternal care during infancy serves to "program" behavioral responses to stress in the offspring by altering the development of the neural systems that mediate fearfulness.
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                Author and article information

                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                18 March 2013
                2013
                : 7
                : 21
                Affiliations
                Department of Psychology, University of California, Davis Davis, CA, USA
                Author notes

                Edited by: Regina M. Sullivan, Nathan Kline Institute, USA

                Reviewed by: Igor Branchi, Istituto Superiore di Sanita, Italy; Elizabeth Hammock, Vanderbilt University, USA

                *Correspondence: Allison M. Perkeybile, Department of Psychology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA. e-mail: aperkeybile@ 123456ucdavis.edu
                Article
                10.3389/fnbeh.2013.00021
                3600544
                23515227
                d0945762-d7e1-48f9-93e6-f97d40794898
                Copyright © 2013 Perkeybile, Griffin and Bales.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 27 October 2012
                : 01 March 2013
                Page count
                Figures: 7, Tables: 6, Equations: 0, References: 73, Pages: 16, Words: 12159
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                affiliation,alloparenting,natural variation,parental care,social behavior
                Neurosciences
                affiliation, alloparenting, natural variation, parental care, social behavior

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