Cited by 162Memory and Neural MechanismsNeurogenesis and neuroplasticity mechanismsStress Responses and Cortisol

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Effects of environmental enrichment on cognitive function and hippocampal NGF in the non-handled rats

Pham, Therese M, Söderström, Stine, Winblad, Bengt, Mohammed, Abdul H·1999·Behavioural Brain Research

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Abstract

In this study we examine whether exposure to differential housing after weaning would counteract the effects of postnatal handling (H) or nonhandling (NH) treatment by affecting learning and memory processes in young rats. In addition, we seek to determine if experience in enriched environment would alter hippocampal nerve growth factor (NGF) levels which is one of the factors known to be involved in the regulation of the survival and differentiation of developing basal forebrain neurones. Rats were either exposed to handling treatment, or left undisturbed starting day 1 after birth through day 21. After weaning on day 22, we exposed half of the H rats and half of the NH rats to environmental enrichment for 60 days. The other respective half of the rats was housed in isolated environmental condition (IC). Behavioural measures were taken in open field test, and spatial water maze test. Exposure to enriched environment following postnatal handling and nonhandling increased hippocampal NGF levels, and improved cognitive function in the both groups, with NH rats being more responsive to the effects of enrichment. Our results suggest that environmental enrichment has the potential to prevent or reduce the cognitive and neurochemical deficits in the adult animals associated with nonhandling.

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Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
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Effect of Neonatal Handling on Age-Related Impairments Associated with the Hippocampus
Meaney, M. J., Aitken, D. H., van Berkel, C., Bhatnagar, S., & Sapolsky, R. M. (1988) · Science · doi:10.1126/science.3340858 · Cited by 1,074
Physiological and behavioral effects of infantile stimulation
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Meaney, M. J., Mitchell, J. B., Aitken, D. H., Bhatnagar, S., Bodnoff, S. R., Iny, L. J., & Sarrieau, A. (1991) · Psychoneuroendocrinology · doi:10.1016/0306-4530(91)90072-2 · Cited by 372
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Einon, D. F., & Morgan, M. J. (1977) · Developmental Psychobiology · doi:10.1002/dev.420100205 · Cited by 342
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Finger, S. (1978) · Springer eBooks · doi:10.1007/978-1-4615-7723-2 · Cited by 322

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References
Young, R. J. (2003) · Wiley eBooks · doi:10.1002/9780470751046.refs
Hippocampal CA1 cytoarchitecture and behaviour after combined neonatal cholinergic lesion and environmental enrichment in rats
Fréchette, M. (2007) · doi:10.22215/etd/2007-07589
The impact of isolation on brain health
Heng, V., Haney, C. W., & Smeyne, R. J. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85654-6.00024-1
Hippocampal plasticity underlying learning and memory processes in healthy and diseased conditions
Petsophonsakul, P. (2017) · theses.fr (ABES) · doi:10.70675/5fdda64ez871dz42c8za517zf44c3618705e
Stratégies non pharmacologiques et réponse aux antidépresseurs dans un modèle murin de dépression : effets comportementaux et mécanismes neurobiologiques
Coutens, B. (2022) · theses.fr (ABES) · doi:10.70675/7ffbfd7ezefb5z4e4ez82f4z42a6ac0ff754
Efeitos da desnutrição proteica pós-natal no funcionamento do eixo hipotálamo-hipófise-adrenal em ratos submetidos ao enriquecimento ambiental
Soares, R. D. O. (2013) · doi:10.11606/t.59.2013.tde-13112013-094352

Authors: Pham, T. M., Söderström, S., Winblad, B., & Mohammed, A. H.
Affiliations: Karolinska Institutet (SE)
Uppsala University (SE)
Corresponding author: Pham, Therese M
ORCID: Pham, Therese M
Winblad, Bengt
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 1999-08
Volume: 103
Issue: 1
Pages: 63-70
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/s0166-4328(99)00019-4
OpenAlex: W1998738051
Cited by: 162
References: 37
Citations by year: 2026: 1 · 2025: 2 · 2024: 1 · 2023: 6 · 2022: 7 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 2 · 2015: 5 · 2014: 11 · 2013: 5 · 2012: 8
FWCI: 2.77
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: Vetenskapsrådet
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: environmental enrichment, postnatal handling, cognitive function, learning and memory, spatial learning, differential housing, individual housing, brain development, open field behavior
MeSH terms: Animals, Cognition, Environment, Female, Handling, Psychological, Hippocampus, Hypothalamus, Motor Activity, Nerve Growth Factors, Pregnancy, Rats, Sprague-Dawley, Maze Learning, Rats

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Effects of environmental enrichment on cognitive function and hippocampal NGF in the non-handled rats

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