Cited by 208Neurogenesis and neuroplasticity mechanismsStress Responses and CortisolMemory and Neural Mechanisms

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Early Stress Evokes Age-Dependent Biphasic Changes in Hippocampal Neurogenesis, Bdnf Expression, and Cognition

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Suri, Deepika, Veenit, Vandana, Sarkar, Ambalika, Thiagarajan, Devi, Kumar, Arvind, Nestler, Eric J., Galande, Sanjeev, Vaidya, Vidita A.·2013·Biological Psychiatry

DOI 10.1016/j.biopsych.2012.10.023PMC PMC4051354

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Abstract

Background Adult-onset stressors exert opposing effects on hippocampal neurogenesis and cognition, with enhancement observed following mild stress and dysfunction following severe chronic stress. While early life stress evokes persistent changes in anxiety, it is unknown whether early stress differentially regulates hippocampal neurogenesis, trophic factor expression, and cognition across the life span.Methods Hippocampal-dependent cognitive behavior, neurogenesis, and epigenetic regulation of brain-derived neurotrophic factor (Bdnf) expression was examined at distinct time points across the life span in rats subjected to the early stress of maternal separation (ES) and control groups. We also examined the influence of chronic antidepressant treatment on the neurogenic, neurotrophic, and cognitive changes in middle-aged ES animals.Results Animals subjected to early stress of maternal separation examined during postnatal life and young adulthood exhibited enhanced hippocampal neurogenesis, decreased repressive histone methylation at the Bdnf IV promoter along with enhanced BDNF levels, and improved performance on the stress-associated Morris water maze. Strikingly, opposing changes in hippocampal neurogenesis and epigenetic regulation of Bdnf IV expression, concomitant with impairments on hippocampal-dependent cognitive tasks, were observed in middle-aged ES animals. Chronic antidepressant treatment with amitriptyline attenuated the maladaptive neurogenic, epigenetic, transcriptional, and cognitive effects in middle-aged ES animals.Conclusions Our study provides novel insights into the short- and long-term consequences of ES, demonstrating both biphasic and unique, age-dependent changes at the molecular, epigenetic, neurogenic, and behavioral levels. These results indicate that early stress may transiently endow animals with a potential adaptive advantage in stressful environments but across a life span is associated with long-term deleterious effects.

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Authors: Suri, D., Veenit, V., Sarkar, A., Thiagarajan, D., Kumar, A., Nestler, E. J., Galande, S., & Vaidya, V. A.
Affiliations: Tata Institute of Fundamental Research (IN)
Centre for Cellular and Molecular Biology (IN)
Icahn School of Medicine at Mount Sinai (US)
Indian Institute of Science Education and Research Pune (IN)
Corresponding author: Vaidya, Vidita A.
ORCID: Suri, Deepika
Sarkar, Ambalika
Kumar, Arvind
Nestler, Eric J.
Galande, Sanjeev
Vaidya, Vidita A.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2013-04
Volume: 73
Issue: 7
Pages: 658-666
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2012.10.023
PMC: PMC4051354
OpenAlex: W2121984222
Cited by: 208
References: 58
Citations by year: 2026: 8 · 2025: 9 · 2024: 11 · 2023: 15 · 2022: 7 · 2021: 13 · 2020: 16 · 2019: 15 · 2018: 16 · 2017: 19 · 2016: 26 · 2015: 23 · 2014: 24 · 2013: 6
FWCI: 5.70
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Wellcome Trust
National Institute of Mental Health (P50MH096890)
National Institute on Drug Abuse (R01DA014133)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: early life stress, maternal separation, hippocampal neurogenesis, BDNF expression, histone methylation, epigenetic regulation, BDNF isoforms, amitriptyline, antidepressant treatment, age-dependent effects, chronic stress
MeSH terms: Aging, Amitriptyline, Animals, Animals, Newborn, Antidepressive Agents, Tricyclic, Cognition, Hippocampus, Male, Maternal Deprivation, Maze Learning, Brain-Derived Neurotrophic Factor, Epigenesis, Genetic, Rats, Neurogenesis

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Early Stress Evokes Age-Dependent Biphasic Changes in Hippocampal Neurogenesis, Bdnf Expression, and Cognition

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