The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey
Abstract
Long-term effects of early experiences have been well documented in rodents, non-human primates and humans. The influence of early experiences on the regulation of the hypothalamic-pituitary-adrenal has demonstrated that this biological system is highly plastic and is permanently modified by early experiences. The effects of brief periods of maternal separation in rodents tend to result in a reduction of the stress response, whereas longer periods of maternal separation produce an animal that is hyperresponsive. The effect of disruptions of mother-infant interactions on the HPA axis in non-human primates has not been clearly established. However, the primate research has primarily focused on more permanent separation paradigms and thus it is difficult to compare the rodent studies with those conducted in primates. The present study attempted to use a separation procedure in monkeys that more closely resembled the rodent model. Intermittent separation during infancy followed by reunion with the mother were shown to lead to a significant reduction in both the cortisol response and the response of the noradrenergic system following social isolation in juvenile squirrel monkeys at 2 and 3 years of age. The behavioral response (vocalizations) was also reduced.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The association between subjective social isolation and gene expression corresponds well to gene expression differences in animal models of social isolation, suggesting that a subjective sense of social connectedness is important for genomic expression and normal immunoregulation in humans.
“However, the association between subjective social isolation and gene expression corresponds well to gene expression differences in animal models of social isolation (e.g., [77–79]), suggesting that a subjective sense of social connectedness is important for genomic expression and normal immunoregulation in humans.”
From Loneliness matters: a theoretical and empirical review of consequences and mechanisms (2010) · cites this paper as [77]
Citations
Cites
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
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638
Flagged first, then by citations
Research works printed but not linked: 17
- Huot, 2001, Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment, Psychopharmacology (Berl), 158, 366, 10.1007/s002130100701 · DOI
- Lehmann, 2000, Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?, Rev Neurosci, 11, 383, 10.1515/REVNEURO.2000.11.4.383 · DOI
- Pryce, 2001, Comparison of the effects of infant handling, isolation, and nonhandling on acoustic startle, prepulse inhibition, locomotion, and HPA activity in the adult rat, Behav Neurosci, 115, 71, 10.1037/0735-7044.115.1.71 · DOI
- Ladd, 2000, Long-term behavioral and neuroendocrine adaptations to adverse early experience, Prog Brain Res, 122, 81, 10.1016/S0079-6123(08)62132-9 · DOI
- Wiener, 1987, Influence of postnatal rearing conditions on the response of squirrel monkey infants to brief perturbations in mother–infant relationships, Physiol Behav, 39, 21, 10.1016/0031-9384(87)90339-8 · DOI
- Hennessy, 1986, Multiple, brief maternal separations in the squirrel monkey: changes in hormonal and behavioral responsiveness, Physiol Behav, 36, 245, 10.1016/0031-9384(86)90011-9 · DOI
- Wiener, 1990, Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus), Behav Neurosci, 104, 108, 10.1037/0735-7044.104.1.108 · DOI
- Suomi, 1983, Models of depression in primates, Psychol Med, 13, 465, 10.1017/S0033291700047887 · DOI
- Faull, 1979, Selected ion monitoring assay for biogenic amine metabolites and probenecid in human lumbar cerebrospinal fluid, J Chromatogr, 163, 337, 10.1016/S0378-4347(00)81637-0 · DOI
- Heim, 2001, Altered pituitary–adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse, Am J Psychiatry, 158, 575, 10.1176/appi.ajp.158.4.575 · DOI · Paper page
- Sanchez, 2001, Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models, Dev Psychopathol, 13, 419, 10.1017/S0954579401003029 · DOI · Paper page
- Francis, 1999, Maternal care, gene expression, and the development of individual differences in stress reactivity, Ann NY Acad Sci, 896, 66, 10.1111/j.1749-6632.1999.tb08106.x · DOI
- Levine, 1988, Psychoendocrine aspects of mother–infant relationships in nonhuman primates, Psychoneuroendocrinology, 13, 143, 10.1016/0306-4530(88)90011-X · DOI
- Ladd, 1996, Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation, Endocrinology, 137, 1212, 10.1210/en.137.4.1212 · DOI
- Patchev, 1997, Neonatal treatment of rats with the neuroactive steroid tetrahydrodeoxycorticosterone (THDOC) abolishes the behavioral and neuroendocrine consequences of adverse early life events, J Clin Invest, 99, 962, 10.1172/JCI119261 · DOI
- Gunnar, 2001, Low cortisol and a flattening of expected daytime rhythm: potential indices of risk in human development, Dev Psychopathol, 13, 515, 10.1017/S0954579401003066 · DOI · Paper page
- Lyons, 2000, Early environmental regulation of glucocorticoid feedback sensitivity in young adult monkeys, J Neuroendocrinol, 12, 723, 10.1046/j.1365-2826.2000.00505.x · DOI
Cited by
Sorted by citations
Loneliness matters: a theoretical and empirical review of consequences and mechanisms
Hawkley, L. C., & Cacioppo, J. T. (2010) · Annals of Behavioral Medicine · doi:10.1007/s12160-010-9210-8 · Cited by 4,782
“, [77–79]), suggesting that a subjective sense of social connectedness is important for genomic expression and normal immunoregulation in humans.”
Resilience as a dynamic concept
Rutter, M. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000028 · Cited by 1,853
Social regulation of gene expression in human leukocytes
Cole, S. W., Hawkley, L. C., Arevalo, J. M., Sung, C. Y., Rose, R. M., & Cacioppo, J. T. (2007) · Genome Biology · doi:10.1186/gb-2007-8-9-r189 · Cited by 745
“This study's identification of a plausible neuroendocrine mediator of transcriptional alteration (GR signaling), which is known to relate to social phenotype in humans [27-30] and is causally impacted by experimental social isolation in animal models [11-14], is consistent with social influences on gene expression.”
BackgroundResultAnnual research review: resilience—clinical implications
Rutter, M. (2013) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2012.02615.x · Cited by 597
Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.008 · Cited by 579
Stress Hormone Regulation: Biological Role and Translation into Therapy
Holsboer, F., & Ising, M. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100321 · Cited by 473
Dozier, M., Peloso, E., Lewis, E., Laurenceau, J.-P., & Levine, S. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000400 · Cited by 377
Self-citationEffects of social isolation on glucocorticoid regulation in social mammals
Hawkley, L. C., Cole, S. W., Capitanio, J. P., Norman, G. J., & Cacioppo, J. T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.011 · Cited by 262
Parker, K. J., Buckmaster, C. L., Sundlass, K., Schatzberg, A. F., & Lyons, D. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506571103 · Cited by 202
Sánchez, M. M., Noble, P. M., Lyon, C. K., Plotsky, P. M., Davis, M., Nemeroff, C. B., & Winslow, J. T. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.11.032 · Cited by 178
Developmental cascades linking stress inoculation, arousal regulation, and resilience
Lyons, D. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.032.2009 · Cited by 163
Brief report: theatre as therapy for children with autism spectrum disorder
Corbett, B. A., Gunther, J. R., Comins, D., Price, J., Ryan, N., Simon, D., Schupp, C. W., & Rios, T. (2011) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-1064-1 · Cited by 160
Social scaffolding of human amygdala-mPFCcircuit development
Tottenham, N. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087424 · Cited by 112
Neisewander, J. L., Peartree, N. A., & Pentkowski, N. S. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2853-3 · Cited by 87
Hagan, M. J., Roubinov, D. S., Purdom Marreiro, C. L., & Luecken, L. J. (2014) · Developmental Psychobiology · doi:10.1002/dev.21157 · Cited by 34
Metadata
- Authors
- Levine, S., & Mody, T.
- Affiliations
- University of California, Davis (US)
- Stanford University (US)
- Corresponding author
- Levine, Seymour
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2003-01
- Volume
- 27
- Issue
- 1-2
- Pages
- 83-89
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2027450460
- Cited by
- 107
- References
- 2
- Citations by year
- 2026: 1 · 2025: 4 · 2023: 3 · 2022: 4 · 2020: 2 · 2019: 5 · 2018: 2 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 5 · 2013: 4 · 2012: 8
- FWCI
- 1.62
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH-1196, K05MH001196)
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-0281)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Keywords
- maternal separation, squirrel monkey, hypothalamic-pituitary-adrenal axis, cortisol response, noradrenergic system, social isolation, early life experience, mother-infant interaction, stress response, vocalizations, long-term effects
- MeSH terms
- Animals, Animals, Newborn, Behavior, Animal, Blood Chemical Analysis, Dependency, Psychological, Female, Homovanillic Acid, Hydrocortisone, Hydroxyindoleacetic Acid, Macaca mulatta, Male, Maternal Deprivation, Methoxyhydroxyphenylglycol, Vocalization, Animal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review