Maternal modulation of novelty effects on physical development

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 6, 2012, Pages 2120-2125

  Tang, Akaysha C ^a,b   Yang, Zhen ^a   Reeb Sutherland, Bethany C ^a,c   Romeo, Russell D ^d   McEwen, Bruce S ^e  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d Barnard College of Columbia University   (United States)

^e ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Developmental plasticity; Growth enhancement; Maternal care; Maternal mediation; Maternal stress

Indexed keywords

CORTICOSTERONE; EARLY GROWTH RESPONSE FACTOR;

ARTICLE; BODY WEIGHT; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; FORCED SWIMMING TEST; HORMONE RESPONSE; MOTHER; NONHUMAN; PHYSICAL DEVELOPMENT; POSTNATAL CARE; PRIORITY JOURNAL; PROGENY; RELIABILITY;

ANIMALS; BODY WEIGHT; EXPLORATORY BEHAVIOR; FEMALE; GROWTH AND DEVELOPMENT; MALE; MATERNAL BEHAVIOR; MEMORY, SHORT-TERM; RATS; STRESS, PSYCHOLOGICAL; WEANING;

EID: 84863115560     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1121056109     Document Type: Article

References (53)

1. Bowlby J (1969) Attachment and Loss (Basic Books, New York).
2. Ainsworth MDS, Blehar MC, Waters E, Wall S (1978) Patterns of Attachment: A Psychological Study of the Strange Situation (Lawrence Erlbaum, Hillsdale, NJ).
3. Rutter M (1981) Maternal Deprivation Reassessed (Penguin books, England), 2nd Ed.
4. Pryce CR, Feldon J (2003) Long-term neurobehavioural impact of the postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 27:57-71. (Pubitemid 36535390)
5. Tang AC, Akers KG, Reeb BC, Romeo RD, McEwen BS (2006) Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proc Natl Acad Sci USA 103:15716-15721. (Pubitemid 44625658)
6. Catalani A, Alemà GS, Cinque C, Zuena AR, Casolini P (2011) Maternal corticosterone effects on hypothalamus-pituitary-adrenal axis regulation and behavior of the offspring in rodents. Neurosci Biobehav Rev 35:1502-1517.
7. Macrì S, Zoratto F, Laviola G (2011) Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother-offspring hormonal transfer. Neurosci Biobehav Rev 35:1534-1543.
8. Liu D, et al. (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic- pituitary-adrenal responses to stress. Science 277:1659-1662. (Pubitemid 27446227)
9. Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155-1158.
10. Russell P (1971) Infantile stimulation in rodents: A consideration of possible mechanisms. Psychol Bull 75:192-202.
11. Parker KJ, Buckmaster CL, Sundlass K, Schatzberg AF, Lyons DM (2006) Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci USA 103:3000-3005.
12. Smotherman WP (1983) Mother-infant interaction and the modulation of pituitary-adrenal activity in rat pups after early stimulation. Dev Psychobiol 16:169-176.
13. Stanton ME, Levine S (1990) Inhibition of infant glucocorticoid stress response: Specific role of maternal cues. Dev Psychobiol 23:411-426. (Pubitemid 20368142)
14. Moriceau S, Sullivan RM (2006) Maternal presence serves as a switch between learning fear and attraction in infancy. Nat Neurosci 9:1004-1006. (Pubitemid 44264911)
15. Akers KG, et al. (2008) Social competitiveness and plasticity of neuroendocrine function in old age: Influence of neonatal novelty exposure and maternal care reliability. PLoS ONE 3:e2840.
16. Reeb-Sutherland BC, Tang AC (2012) Functional specificity in the modulation of novelty exposure effects by reliability of maternal care. Behav Brain Res 226:345-350.
17. Tang AC, Reeb-Sutherland BC, Yang Z, Romeo RD, McEwen BS (2011) Neonatal novelty-induced persistent enhancement in offspring spatial memory and the modulatory role of maternal self-stress regulation. J Neurosci 31:5348-5352.
18. Tang AC, et al. (2011) Converging influence of neonatal novelty experience and maternal self-stress regulation on the plasticity of offspring acoustic startle response latency. Behav Brain Res 221:253-260.
19. Essex MJ, et al. (2006) Exploring risk factors for the emergence of children's mental health problems. Arch Gen Psychiatry 63:1246-1256. (Pubitemid 44708083)
20. Glover V, O'Connor TG, O'Donnell K (2010) Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 35:17-22.
21. Gunnar MR, Brodersen L, Nachmias M, Buss K, Rigatuso J (1996) Stress reactivity and attachment security. Dev Psychobiol 29:191-204. (Pubitemid 126482317)
22. Nachmias M, Gunnar M, Mangelsdorf S, Parritz RH, Buss K (1996) Behavioral inhibition and stress reactivity: The moderating role of attachment security. Child Dev 67:508-522. (Pubitemid 126420287)
23. Leerkes EM (2011) Maternal sensitivity during distressing tasks: A unique predictor of attachment security. Infant Behav Dev 34:443-446.
24. Thelen E, Smith LB (1994) A Dynamic Systems Approach to the Development of Cognition and Action (MIT Press, Cambridge MA).
25. Boyce WT, Ellis BJ (2005) Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17:271-301. (Pubitemid 41388314)
26. Phillips DA, Fox NA, Gunnar MR (2011) Same place, different experiences: Bringing individual differences to research in child care. Child Dev Perspect 5:44-49.
27. World Health Organization (2006) WHO child growth standards: Length/height-forage, weight-for-age, weight-for-length, weight-for-height and body mass index-forage: methods and development. (WHO, Geneva), p 312.
28. UNICEF, WHO (2004) Low Birthweight: Country, Regional and Global Estimates (WHO, Geneva), p. 27.
29. Dallman MF (2010) Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab 21:159-165.
30. Levine S (1960) Stimulation in infancy. Sci Am 202:81-86.
31. Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161-1192.
32. Zou B, Golarai G, Connor JA, Tang AC (2001) Neonatal exposure to a novel environment enhances the effects of corticosterone on neuronal excitability and plasticity in adult hippocampus. Brain Res Dev Brain Res 130:1-7. (Pubitemid 32830967)
33. Denenberg VH (1964) Critical periods, stimulus input, and emotional reactivity: A theory of infantile stimulation. Psychol Rev 71:335-351.
34. Levine S (1962) Plasma-free corticosteroid response to electric shock in rats stimulated in infancy. Science 135:795-796.
35. Champagne FA, Francis DD, Mar A, Meaney MJ (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359-371. (Pubitemid 37098279)
36. Daly M (1973) Early stimulation of rodents: A critical review of present interpretations. Br J Psychol 64:435-460.
37. Gunnar MR, Talge NM, Herrera A (2009) Stressor paradigms in developmental studies: What does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology 34:953-967.
38. Tang AC, Reeb-Sutherland BC, Yang Z (2011) Functional brain asymmetry in adult novelty response: On fluidity of neonatal novelty exposure effects. Behav Brain Res 221:91-97.
39. Yang Z, Tang AC (2011) Novelty-induced enhancement in spatial memory: Is infancy a critical period? Behav Brain Res 219:47-54.
40. Rutter M English and Romanian Adoptees (ERA) Study Team (1998) Developmental catch-up, and deficit, following adoption after severe global early privation. J Child Psychol Psychiatry 39:465-476.
41. van Ijzendoorn MH, Juffer F (2006) The Emanuel Miller Memorial Lecture 2006: Adoption as intervention. Meta-analytic evidence for massive catch-up and plasticity in physical, socio-emotional, and cognitive development. J Child Psychol Psychiatry 47:1228-1245. (Pubitemid 44824719)
42. Barker D (2007) The developmental origins of obesity. Obesity: Epidemiology, Etiology, Consequences and Treatment, ed Bouchard C (Henry Stewart Talks Ltd, London).
43. Hughes PCR, Tanner JM (1970) A longitudinal study of the growth of the blackhooded rat: Methods of measurement and rates of growth for skull, limbs, pelvis, nose-rump and tail lengths. J Anat 106:349-370.
44. Ainsworth MDS (1963) The development of infant-mother interaction among the Ganda. Determinants of Infant Behavior, ed Foss BM (Wiley, New York), pp 67-104.
45. Hane AA, Fox NA (2006) Ordinary variations in maternal caregiving influence human infants' stress reactivity. Psychol Sci 17:550-556. (Pubitemid 43855801)
46. Macrí S, Mason GJ, Würbel H (2004) Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur J Neurosci 20:1017-1024.
47. Ragan CM, Loken E, Stifter CA, Cavigelli SA (2012) Within-litter variance in early pupmother interactions and adult offspring responses to novelty. Dev Psychobiol, 10.1002/dev.20581.
48. Mischel W (2009) From personality and assessment (1968) to personality science. J Res Pers 43:282-290.
49. Pluess M, Belsky J (2009) Differential susceptibility to rearing experience: The case of childcare. J Child Psychol Psychiatry 50:396-404.
50. Smith E, Collins E (2010) Situated cognition. The Mind in Context, eds Mesquita B, Barrett LF, Smith E (Guilford, New York).
51. Gluckman PD, Hanson MA (2004) Living with the past: Evolution, development, and patterns of disease. Science 305:1733-1736. (Pubitemid 39249632)
52. Hinde RA (1986) Some implications of evolutionary theory and comparative data for the study of human prosocial and aggressive behavior. Development of Anti-Social and Prosocial Behaviour, eds Olweus D, Block J, Radke-Yarrow M (Academic Press, Orlando, FL).
53. Rossiter MC (1999) The role of environmental variation in parental effects expression. Maternal Effects as Adaptations, eds Mousseau TA, Fox CW (Oxford University Press, London).