The DOI matches its Crossref record, with a small difference in title or year; 134 of the 137 references it cites were found in a registry or an index.
Early-life handling stimulation and environmental enrichment
Abstract
Neonatal (early) handling (EH) and environmental enrichment (EE) of laboratory rodents have been the two most commonly used methods of providing supplementary environmental stimulation in order to study behavioral and neurobiological plasticity. A large body of research has been generated since the 1950s, unequivocally showing that both treatments induce profound and long-lasting behavioral and neural consequences while also inducing plastic brain effects and being "protective" against some age-related deficits. The present work is aimed at reviewing the main neurobehavioral effects of both manipulations, with the final purpose of comparing them and trying to find out to what extent the effects of both treatments may share (or not) possible neural mechanisms.
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“The findings of Francis et al. (2002) and Bredy et al. (2003) indicate that the effects of enrichment as seen at the behavioral level are not necessarily mirrored in expected changes at the biological level (Fernandez-Teruel et al., 2002).”
From Stress and the development of self-regulation in context (2010) · cites this paper as Fernandez-Teruel et al., 2002
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Cites
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984
More hippocampal neurons in adult mice living in an enriched environment
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997) · Nature · doi:10.1038/386493a0 · Cited by 3,586
Neural consequences of enviromental enrichment
van Praag, H., Kempermann, G., & Gage, F. H. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044558 · Cited by 2,468
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
Psychobiology of plasticity: Effects of training and experience on brain and behavior
Rosenzweig, M. R., & Bennett, E. L. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00216-2 · Cited by 972
(1992) · Cited by 777
Validity of head-dipping as a measure of exploration in a modified hole-board
File, S. E., & Wardill, A. G. (1975) · Psychopharmacology · doi:10.1007/bf00421184 · Cited by 670
Psychobiology of novelty seeking and drug seeking behavior
Bardo, M. T., Donohew, R. L., & Harrington, N. G. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00203-0 · Cited by 667
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659
Research works printed but not linked: 4
- Ader, 1959, The effects of early experience on subsequent emotionality and resistance to stress, Psychol Monogr, 73
- Fernández-Teruel, 2000, Phospholipase C (PLC) beta1 levels in brain cortical membranes from RHA/Verh and RLA/Verh rats: effects of aging and neonatal handling, Eur J Neurosci, 12, 6
- Hargreaves, 1992, Rats housed in a complex environment exhibit greater hilar LTP than individually housed littermates, Soc Neurosci Abstr, 18, 344
- Núñez JF. Effects of infantile stimulation on anxiety in rats: behavioral, physiological and neurochemical measures. Doctoral dissertation (microfilm). Barcelona: Publications of UAB, 1997.
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Cuenya, L., Sabariego, M., Donaire, R., Callejas-Aguilera, J. E., Torres, C., & Fernández‐Teruel, A. (2016) · Behavioural Processes · doi:10.1016/j.beproc.2016.02.003 · Cited by 8
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Simpson, J. (2011) · ARAN (University of Galway Research Repository) (Ollscoil na Gaillimhe – University of Galway) · doi:10.13025/17838 · Cited by 1
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Seetharaman, S. (2009) · Digital Commons - University of South Florida (University of South Florida)
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Zhu, S. (2006) · Figshare
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Pereira, L. O., & Silva, P. (2007)
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Metadata
- Authors
- Fernández-Teruel, A., Giménez-Llort, L., Escorihuela, R. M., Gil, L., Aguilar, R., Steimer, T., & Tobeña, A.
- Affiliations
- Universitat Autònoma de Barcelona (ES)
- Venue
- Pharmacology Biochemistry and Behavior
- Publisher
- Elsevier BV
- Published
- 2002-08
- Volume
- 73
- Issue
- 1
- Pages
- 233-245
- ISSN
- 0091-3057 (ISSN-L)
- OpenAlex
- W80710638
- Cited by
- 171
- References
- 137
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 6 · 2019: 8 · 2018: 7 · 2017: 8 · 2016: 5 · 2015: 11 · 2014: 8 · 2013: 7 · 2012: 7
- FWCI
- 0.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Pharmacology Biochemistry and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- neonatal handling, environmental enrichment, laboratory rodents, neuroplasticity, behavioral plasticity, neurobehavioral effects, brain development, age-related deficits, neural mechanisms
- MeSH terms
- Animals, Animals, Newborn, Environment, Exploratory Behavior, Handling, Psychological, Learning, Rats
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