Cited by 484Stress Responses and CortisolNeuroendocrine regulation and behaviorMemory and Neural Mechanisms

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Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long–Evans rats

Kalinichev, Mikhail, Easterling, Keith W, Plotsky, Paul M, Holtzman, Stephen G·2002·Pharmacology Biochemistry and Behavior

DOI 10.1016/s0091-3057(02)00781-5

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Abstract

Early neonatal environmental factors appear to have powerful and long-lasting influences on an organism's physiology and behavior. Long-Evans male rats separated from their dam for 3 h daily over the first 2 weeks of life (maternally separated, MS rats) when tested as adults exhibit exaggerated behavioral and neuroendocrine responses to stress compared to 15-min separated (handled, H) animals. The purpose of this study was to compare male and female adult rats that were MS, H or were undisturbed (nonhandled, NH) as neonates in anxiety-like behaviors, in the elevated plus-maze, and in response to startle-inducing auditory stimuli. We confirmed that MS males oversecrete corticosterone (CORT; 2.5-5 times) in response to mild handling stress. MS males and females were less likely to explore open arms of the plus-maze. MS males exhibited 35% higher startle amplitudes compared to controls. Furthermore, MS males were more likely to emit ultrasonic vocalizations in response to startle than were H controls. However, MS and control females did not differ in auditory startle response or in startle-induced ultrasonic vocalizations. Therefore, experiencing maternal separation results in a long-lasting increase in anxiety-like behaviors that occurs in a sex-dependent manner.

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Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822
The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders
Heim, C., Ehlert, U., & Hellhammer, D. H. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00035-9 · Cited by 1,688
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638
Self-citation
Anxiety, defence and the elevated plus-maze.
Rodgers, R., & Dalvi, A. (1997) · Neuroscience and Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00058-9 · Cited by 1,028
Maternal behavior in mammals.
Rheingold, H. L. (1963) · Medical Entomology and Zoology · Cited by 879
Ethopharmacological analysis of rat behavior on the elevated plus-maze
Cruz, A. P. D. M., Frei, F., & Graeff, F. G. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90472-3 · Cited by 822
Prenatal Stress Induces High Anxiety and Postnatal Handling Induces Low Anxiety in Adult Offspring: Correlation with Stress-Induced Corticosterone Secretion
Vallée, M., Mayo, W., Dellu-Hagedorn, F., Moal, M. L., Simon, H., & Maccari, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02626.1997 · Cited by 787
Long-term behavioral and neuroendocrine adaptations to adverse early experience
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62132-9 · Cited by 726
Self-citation
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659
The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat
Caldji, C., Francis, D., Sharma, S., Plotsky, P., & Meaney, M. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 600

Show all 56 references

Research works printed but not linked: 1

Huot, 1997, Alterations of maternal–infant interaction as a results of maternal separation in Long–Evans rats and its behavioral and neuroendocrine consequences, Psychoneuroendocrinology, 22, S173

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The Behavioral and Immunological Impact of Maternal Separation: A Matter of Timing
Roque, S., Mesquita, A. R., Palha, J. A., Sousa, N., & Correia‐Neves, M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00192 · Cited by 91
Long-lasting consequences of neonatal maternal separation on social behaviors in ovariectomized female mice.
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Authors: Kalinichev, M., Easterling, K. W., Plotsky, P. M., & Holtzman, S. G.
Affiliations: Emory University (US)
Corresponding author: Kalinichev, Mikhail
ORCID: Kalinichev, Mikhail
Venue: Pharmacology Biochemistry and Behavior
Publisher: Elsevier BV
Published: 2002-08
Volume: 73
Issue: 1
Pages: 131-140
ISSN: 0091-3057 (ISSN-L)
DOI: 10.1016/s0091-3057(02)00781-5
OpenAlex: W2055408622
Cited by: 484
References: 56
Citations by year: 2026: 9 · 2025: 3 · 2024: 12 · 2023: 16 · 2022: 18 · 2021: 18 · 2020: 19 · 2019: 23 · 2018: 20 · 2017: 15 · 2016: 20 · 2015: 17 · 2014: 40 · 2013: 30 · 2012: 27
FWCI: 6.88
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Pharmacology Biochemistry and Behavior (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute on Drug Abuse (K05-DA00008, DA11384, K05DA000008, R21DA011384)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: neonatal maternal separation, anxiety-like behavior, corticosterone, stress response, sex differences, ultrasonic vocalizations, startle response, elevated plus maze, Long-Evans rats, early life experience, handling stress
MeSH terms: Acoustic Stimulation, Animals, Animals, Newborn, Anxiety, Corticosterone, Female, Male, Maternal Deprivation, Pregnancy, Stress, Physiological, Time, Vocalization, Animal, Rats, Long-Evans, Rats

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Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long–Evans rats

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