Neonatal Novelty-induced Persistent Enhancement in Offspring Spatial Memory and the Modulatory Role of Maternal Self-stress Regulation

Overview

Journal J Neurosci

Specialty Neurology

Date 2011 Apr 8

PMID 21471369

Citations 8

Authors

Akaysha C Tang

Bethany C Reeb-Sutherland

Zhen Yang

Russell D Romeo

Bruce S McEwen

Affiliations

Soon will be listed here.

Abstract

Development of spatial memory in the rat is influenced by both maternal and nonmaternal aspects of the postnatal environment. Yet it remains poorly understood how these two aspects of the postnatal environment interact to program offspring cognitive development. By considering the joint influence of neonatal environmental novelty and maternal self-stress regulation on the development of spatial memory function in Long-Evans hooded rats, we show a persistent neonatal novelty-induced enhancement in spatial reference and working memory functions among the same individual offspring from juvenility to adulthood and a contrasting transient maternal modulatory influence on this novelty-related enhancement present during only juvenility. Specifically, at and only at juvenility, for mothers with good self-stress regulation as indexed by a low circulating basal corticosterone level, offspring showed a novelty-induced enhancement in spatial memory function, whereas for mothers with poor self-stress regulation, indexed by a high basal corticosterone level, offspring showed little enhancement or even small impairments. These findings indicate that maternal and nonmaternal postnatal environments exert separate but interacting influences on offspring cognitive development and support a maternal modulation model of cognitive development that considers maternal self-stress regulation as an important factor among the multitude of maternal influences.

Citing Articles

Why and how the early-life environment affects development of coping behaviours.

Langenhof M, Komdeur J Behav Ecol Sociobiol. 2018; 72(3):34.

PMID: 29449757 PMC: 5805793. DOI: 10.1007/s00265-018-2452-3.

Genetic predisposition to high anxiety- and depression-like behavior coincides with diminished DNA methylation in the adult rat amygdala.

McCoy C, Jackson N, Day J, Clinton S Behav Brain Res. 2016; 320:165-178.

PMID: 27965039 PMC: 5239722. DOI: 10.1016/j.bbr.2016.12.008.

Estrogen Effects on Cognitive and Synaptic Health Over the Lifecourse.

Hara Y, Waters E, McEwen B, Morrison J Physiol Rev. 2015; 95(3):785-807.

PMID: 26109339 PMC: 4491541. DOI: 10.1152/physrev.00036.2014.

Enhancing offspring hypothalamic-pituitary-adrenal (HPA) regulation via systematic novelty exposure: the influence of maternal HPA function.

Dinces S, Romeo R, McEwen B, Tang A Front Behav Neurosci. 2014; 8:204.

PMID: 24926243 PMC: 4046569. DOI: 10.3389/fnbeh.2014.00204.

The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome.

Daskalakis N, Bagot R, Parker K, Vinkers C, de Kloet E Psychoneuroendocrinology. 2013; 38(9):1858-73.

PMID: 23838101 PMC: 3773020. DOI: 10.1016/j.psyneuen.2013.06.008.

References

Tang A, Zou B . Neonatal exposure to novelty enhances long-term potentiation in CA1 of the rat hippocampus. Hippocampus. 2002; 12(3):398-404. DOI: 10.1002/hipo.10017. View

Panakhova E, Buresova O, Bures J . Persistence of spatial memory in the Morris water tank task. Int J Psychophysiol. 1984; 2(1):5-10. DOI: 10.1016/0167-8760(84)90066-7. View

Catalani A, Alema G, Cinque C, Zuena A, Casolini P . Maternal corticosterone effects on hypothalamus-pituitary-adrenal axis regulation and behavior of the offspring in rodents. Neurosci Biobehav Rev. 2010; 35(7):1502-17. DOI: 10.1016/j.neubiorev.2010.10.017. View

Steele R, Morris R . Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus. 1999; 9(2):118-36. DOI: 10.1002/(SICI)1098-1063(1999)9:2<118::AID-HIPO4>3.0.CO;2-8. View

Casolini P, Cigliana G, Alema G, Ruggieri V, Angelucci L, Catalani A . Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life. Neuroscience. 1997; 79(4):1005-12. DOI: 10.1016/s0306-4522(96)00668-9. View

Stanton M, Wallstrom J, Levine S . Maternal contact inhibits pituitary-adrenal stress responses in preweanling rats. Dev Psychobiol. 1987; 20(2):131-45. DOI: 10.1002/dev.420200204. View

Raineki C, Moriceau S, Sullivan R . Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biol Psychiatry. 2010; 67(12):1137-45. PMC: 3929962. DOI: 10.1016/j.biopsych.2009.12.019. View

Barnett S, Burn J . Early stimulation and maternal behaviour. Nature. 1967; 213(5072):150-2. DOI: 10.1038/213150a0. View

Francis D, Diorio J, Liu D, Meaney M . Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science. 1999; 286(5442):1155-8. DOI: 10.1126/science.286.5442.1155. View

10.

Denenberg V . Commentary: is maternal stimulation the mediator of the handling effect in infancy?. Dev Psychobiol. 1999; 34(1):1-3. DOI: 10.1002/(sici)1098-2302(199901)34:1<1::aid-dev2>3.0.co;2-u. View

11.

Whishaw I . Formation of a place learning-set by the rat: a new paradigm for neurobehavioral studies. Physiol Behav. 1985; 35(1):139-43. DOI: 10.1016/0031-9384(85)90186-6. View

12.

Yang Z, Tang A . Novelty-induced enhancement in spatial memory: is infancy a critical period?. Behav Brain Res. 2010; 219(1):47-54. DOI: 10.1016/j.bbr.2010.12.020. View

13.

Parker K, Buckmaster C, Sundlass K, Schatzberg A, Lyons D . Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci U S A. 2006; 103(8):3000-5. PMC: 1413772. DOI: 10.1073/pnas.0506571103. View

14.

Benetti F, Andrade de Araujo P, Sanvitto G, Lucion A . Effects of neonatal novelty exposure on sexual behavior, fear, and stress-response in adult rats. Dev Psychobiol. 2007; 49(3):258-64. DOI: 10.1002/dev.20181. View

15.

Macri S, Wurbel H . Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav. 2006; 50(5):667-80. DOI: 10.1016/j.yhbeh.2006.06.015. View

16.

Joels M, Pu Z, Wiegert O, Oitzl M, Krugers H . Learning under stress: how does it work?. Trends Cogn Sci. 2006; 10(4):152-8. DOI: 10.1016/j.tics.2006.02.002. View

17.

Stanton M, Levine S . Inhibition of infant glucocorticoid stress response: specific role of maternal cues. Dev Psychobiol. 1990; 23(5):411-26. DOI: 10.1002/dev.420230504. View

18.

de Kloet E, Vreugdenhil E, Oitzl M, Joels M . Brain corticosteroid receptor balance in health and disease. Endocr Rev. 1998; 19(3):269-301. DOI: 10.1210/edrv.19.3.0331. View

19.

Akers K, Yang Z, DelVecchio D, Reeb B, Romeo R, McEwen B . Social competitiveness and plasticity of neuroendocrine function in old age: influence of neonatal novelty exposure and maternal care reliability. PLoS One. 2008; 3(7):e2840. PMC: 2475497. DOI: 10.1371/journal.pone.0002840. View

20.

Morris R, Garrud P, Rawlins J, Okeefe J . Place navigation impaired in rats with hippocampal lesions. Nature. 1982; 297(5868):681-3. DOI: 10.1038/297681a0. View