Literature DB >> 17030787

Programming social, cognitive, and neuroendocrine development by early exposure to novelty.

Akaysha C Tang1, Katherine G Akers, Bethany C Reeb, Russell D Romeo, Bruce S McEwen.   

Abstract

Mildly stressful early life experiences can potentially impact a broad range of social, cognitive, and physiological functions in humans, nonhuman primates, and rodents. Recent rodent studies favor a maternal-mediation hypothesis that considers maternal-care differences induced by neonatal stimulation as the cause of individual differences in offspring development. Using neonatal novelty exposure, a neonatal stimulation paradigm that dissociates maternal individual differences from a direct stimulation effect on the offspring, we investigated the effect of early exposures to novelty on a diverse range of psychological functions using several assessment paradigms. Pups that received brief neonatal novelty exposures away from the home environment showed enhancement in spatial working memory, social competition, and corticosterone response to surprise during adulthood compared with their home-staying siblings. These functional enhancements in novelty-exposed rats occurred despite evidence that maternal care was directed preferentially toward home-staying instead of novelty-exposed pups, indicating that greater maternal care is neither necessary nor sufficient for these early stimulation-induced functional enhancements. We suggest a unifying maternal-modulation hypothesis, which distinguishes itself from the maternal-mediation hypothesis in that (i) neonatal stimulation can have direct effects on pups, cumulatively leading to long-term improvement in adult offspring; and (ii) maternal behavior can attenuate or potentiate these effects, thereby decreasing or increasing this long-term functional improvement.

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Year:  2006        PMID: 17030787      PMCID: PMC1622887          DOI: 10.1073/pnas.0607374103

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  41 in total

Review 1.  Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations.

Authors:  M J Meaney
Journal:  Annu Rev Neurosci       Date:  2001       Impact factor: 12.449

2.  Handling rat pups after early weaning.

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Journal:  Behav Biol       Date:  1975-04

3.  Stimulation in infancy.

Authors:  S LEVINE
Journal:  Sci Am       Date:  1960-05       Impact factor: 2.142

Review 4.  Commentary: is maternal stimulation the mediator of the handling effect in infancy?

Authors:  V H Denenberg
Journal:  Dev Psychobiol       Date:  1999-01       Impact factor: 3.038

5.  Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat.

Authors:  C Caldji; B Tannenbaum; S Sharma; D Francis; P M Plotsky; M J Meaney
Journal:  Proc Natl Acad Sci U S A       Date:  1998-04-28       Impact factor: 11.205

6.  Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin.

Authors:  M J Meaney; J Diorio; D Francis; S Weaver; J Yau; K Chapman; J R Seckl
Journal:  J Neurosci       Date:  2000-05-15       Impact factor: 6.167

7.  Neonatal exposure to a novel environment enhances the effects of corticosterone on neuronal excitability and plasticity in adult hippocampus.

Authors:  B Zou; G Golarai; J A Connor; A C Tang
Journal:  Brain Res Dev Brain Res       Date:  2001-09-23

8.  Effect of neonatal handling on age-related impairments associated with the hippocampus.

Authors:  M J Meaney; D H Aitken; C van Berkel; S Bhatnagar; R M Sapolsky
Journal:  Science       Date:  1988-02-12       Impact factor: 47.728

Review 9.  Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress.

Authors:  M J Meaney; J Diorio; D Francis; J Widdowson; P LaPlante; C Caldji; S Sharma; J R Seckl; P M Plotsky
Journal:  Dev Neurosci       Date:  1996       Impact factor: 2.984

10.  Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure.

Authors:  Akaysha C Tang; Bethany C Reeb; Russell D Romeo; Bruce S McEwen
Journal:  J Neurosci       Date:  2003-09-10       Impact factor: 6.167

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  38 in total

1.  Maternal modulation of novelty effects on physical development.

Authors:  Akaysha C Tang; Zhen Yang; Bethany C Reeb-Sutherland; Russell D Romeo; Bruce S McEwen
Journal:  Proc Natl Acad Sci U S A       Date:  2012-01-24       Impact factor: 11.205

2.  Intergenerational transmission of the behavioral consequences of early experience in prairie voles.

Authors:  Anita Iyengar Stone; Karen Lisa Bales
Journal:  Behav Processes       Date:  2010-05-10       Impact factor: 1.777

Review 3.  Animal models of early life stress: Implications for understanding resilience.

Authors:  David M Lyons; Karen J Parker; Alan F Schatzberg
Journal:  Dev Psychobiol       Date:  2010-07       Impact factor: 3.038

Review 4.  Social influences on neuroplasticity: stress and interventions to promote well-being.

Authors:  Richard J Davidson; Bruce S McEwen
Journal:  Nat Neurosci       Date:  2012-04-15       Impact factor: 24.884

Review 5.  Understanding the potency of stressful early life experiences on brain and body function.

Authors:  Bruce S McEwen
Journal:  Metabolism       Date:  2008-10       Impact factor: 8.694

6.  Early rearing experience is associated with vasopressin immunoreactivity but not reactivity to an acute non-social stressor in the prairie vole.

Authors:  Allison M Perkeybile; Karen L Bales
Journal:  Physiol Behav       Date:  2015-04-15

7.  Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition.

Authors:  Deepika Suri; Vandana Veenit; Ambalika Sarkar; Devi Thiagarajan; Arvind Kumar; Eric J Nestler; Sanjeev Galande; Vidita A Vaidya
Journal:  Biol Psychiatry       Date:  2012-12-11       Impact factor: 13.382

8.  Moderate within-person variability in cortisol is related to executive function in early childhood.

Authors:  Clancy Blair; Daniel J Berry
Journal:  Psychoneuroendocrinology       Date:  2017-03-31       Impact factor: 4.905

Review 9.  Transitions in sensitive period attachment learning in infancy: the role of corticosterone.

Authors:  Regina M Sullivan; Parker J Holman
Journal:  Neurosci Biobehav Rev       Date:  2009-11-29       Impact factor: 8.989

10.  Developmental cascades linking stress inoculation, arousal regulation, and resilience.

Authors:  David M Lyons; Karen J Parker; Maor Katz; Alan F Schatzberg
Journal:  Front Behav Neurosci       Date:  2009-09-18       Impact factor: 3.558

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