Social isolation disrupts hippocampal neurogenesis in young non-human primates
Open accessAbstract
Social relationships are crucial for the development and maintenance of normal behavior in non-human primates. Animals that are raised in isolation develop abnormal patterns of behavior that persist even when they are later reunited with their parents. In rodents, social isolation is a stressful event and is associated with a decrease in hippocampal neurogenesis but considerably less is known about the effects of social isolation in non-human primates during the transition from adolescence to adulthood. To investigate how social isolation affects young marmosets, these were isolated from other members of the colony for 1 or 3 weeks and evaluated for alterations in their behavior and hippocampal cell proliferation. We found that anxiety-related behaviors like scent-marking and locomotor activity increased after social isolation when compared to baseline levels. In agreement, grooming-an indicative of attenuation of tension-was reduced among isolated marmosets. These results were consistent with increased cortisol levels after 1 and 3 weeks of isolation. After social isolation (1 or 3 weeks), reduced proliferation of neural cells in the subgranular zone of dentate granule cell layer was identified and a smaller proportion of BrdU-positive cells underwent neuronal fate (doublecortin labeling). Our data is consistent with the notion that social deprivation during the transition from adolescence to adulthood leads to stress and produces anxiety-like behaviors that in turn might affect neurogenesis and contribute to the deleterious consequences of prolonged stressful conditions.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In adolescent non-human primates, deprivation of peer contact for 1-3 weeks results in anxiety-like behaviours and reduced cell proliferation and neurogenesis in hippocampus.
“Although much scarcer, research on the effects of social deprivation in adolescent non-human primates has shown effects in line with the rodent research: deprivation of contact with peers for 1–3 weeks results in anxiety-like behaviours and a reduction in cell proliferation and neurogenesis in the hippocampus (a brain region involved in learning and memory).56”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [56]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants
Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., et al. (2003) · Science · doi:10.1126/science.1083328 · Cited by 4,321 · see citing works
A Neurotrophic Model for Stress-Related Mood Disorders
Duman, R. S., & Monteggia, L. M. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.02.013 · Cited by 3,375 · see citing works
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · see citing works
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853 · see citing works
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · see citing works
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496 · see citing works
Gould, E., Tanapat, P., McEwen, B. S., Flügge, G., & Fuchs, E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3168 · Cited by 1,395 · see citing works
The ascent of mouse: advances in modelling human depression and anxiety
Cryan, J. F., & Holmes, A. (2005) · Nature Reviews Drug Discovery · doi:10.1038/nrd1825 · Cited by 1,198 · see citing works
Kee, N., Teixeira, C. M., Wang, A. H., & Frankland, P. W. (2007) · Nature Neuroscience · doi:10.1038/nn1847 · Cited by 875 · see citing works
IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress
Koo, J. W., & Duman, R. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708092105 · Cited by 862 · see citing works
Malberg, J. E., & Duman, R. S. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300234 · Cited by 815 · see citing works
Mirescu, C., & Gould, E. (2006) · Hippocampus · doi:10.1002/hipo.20155 · Cited by 701 · see citing works
Early life experience alters response of adult neurogenesis to stress
Mirescu, C., Peters, J. D., & Gould, E. (2004) · Nature Neuroscience · doi:10.1038/nn1290 · Cited by 625 · see citing works
Ventral hippocampal lesions affect anxiety but not spatial learning
Bannerman, D. M., Grubb, M., Deacon, R. M. J., Yee, B. K., Feldon, J., & Rawlins, J. N. P. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00268-1 · Cited by 530 · see citing works
Neurogenesis in Adult Mammals: Some Progress and Problems
Gould, E., & Gross, C. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00619.2002 · Cited by 510 · see citing works
Social isolation delays the positive effects of running on adult neurogenesis
Stranahan, A. M., Khalil, D., & Gould, E. (2006) · Nature Neuroscience · doi:10.1038/nn1668 · Cited by 467 · see citing works
Development of a microtitre plate enzyme immunoassay for the determination of progesterone
Munro, C. J., & Stabenfeldt, G. H. (1984) · Journal of Endocrinology · doi:10.1677/joe.0.1010041 · Cited by 453 · see citing works
Balu, D. T., & Lucki, I. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.007 · Cited by 382 · see citing works
Computational Influence of Adult Neurogenesis on Memory Encoding
Aimone, J. B., Wiles, J., & Gage, F. H. (2009) · Neuron · doi:10.1016/j.neuron.2008.11.026 · Cited by 370 · see citing works
Nonhuman primate models for human growth and development
Watts, E. S. (1985) · A.R. Liss eBooks · Cited by 330 · see citing works
Marmosets and tamarins: systematics, behaviour, and ecology
(1994) · Choice Reviews Online · doi:10.5860/choice.31-4916 · Cited by 294 · see citing works
Focused grooming networks and stress alleviation in wild female baboons
Wittig, R. M., Crockford, C., Lehmann, J., Whitten, P. L., Seyfarth, R. M., & Cheney, D. L. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.009 · Cited by 284 · see citing works
From monoamines to genomic targets: a paradigm shift for drug discovery in depression
Wong, M., & Licinio, J. (2004) · Nature Reviews Drug Discovery · doi:10.1038/nrd1303 · Cited by 225 · see citing works
Ziegler, T. E., Scheffler, G., & Snowdon, C. T. (1995) · Hormones and Behavior · doi:10.1006/hbeh.1995.1028 · Cited by 210 · see citing works
Wong, E. Y. H., & Herbert, J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.073 · Cited by 200 · see citing works
Early-life stress mediated modulation of adult neurogenesis and behavior
Korosi, A., Naninck, E. F. G., Oomen, C. A., Schouten, M., Krugers, H., Fitzsimons, C., & Lucassen, P. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.037 · Cited by 194 · see citing works
Opposite effects of early maternal deprivation on neurogenesis in male versus female rats
Oomen, C. A., Girardi, C. E. N., Cahyadi, R., Verbeek, E. C., Krugers, H., Joëls, M., & Lucassen, P. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0003675 · Cited by 190 · see citing works
Wong, E. Y. H., & Herbert, J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04277.x · Cited by 155 · see citing works
2006 Curt P. Richter award winner
DeVries, A. C., Craft, T. K. S., Glasper, E. R., Neigh, G. N., & Alexander, J. K. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.007 · Cited by 153 · see citing works
Biology of Adolescent Behavior and Development
Adams, G. R., Montemayor, R., & Gullotta, T. P. (1989) · Cited by 150 · see citing works
Influences of environmental demand on maternal behavior and infant development
Rosenblum, L. A., & Andrews, M. W. (1994) · Acta Paediatrica · doi:10.1111/j.1651-2227.1994.tb13266.x · Cited by 144 · see citing works
The Brain of the Common Marmoset (Callithrix Jacchus): A Stereotaxic Atlas
Stephan, H., Baron, G., & Schwerdtfeger, W. K. (1980) · Medical Entomology and Zoology · Cited by 142 · see citing works
Jacobsen, J. P. R., & Mørk, A. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.077 · Cited by 139 · see citing works
Dettling, A. C., Feldon, J., & Pryce, C. R. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01460-9 · Cited by 134 · see citing works
Behavioural and physiological aspects of stress and aggression in nonhuman primates
Honess, P. E., & Marin, C. M. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.003 · Cited by 132 · see citing works
The Brain of the Common Marmoset (Callithrix jacchus)
Stephan, H., Schwerdtfeger, W. K., & Baron, G. (1980) · Springer eBooks · doi:10.1007/978-3-642-67491-4 · Cited by 129 · see citing works
Rukstalis, M., & French, J. A. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.09.004 · Cited by 115 · see citing works
Dettling, A. C., Feldon, J., & Pryce, C. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00785-2 · Cited by 113 · see citing works
Ziegler, T. E. (1996) · Biology of Reproduction · doi:10.1095/biolreprod54.1.91 · Cited by 111 · see citing works
Smith, T. E., McGreer-Whitworth, B., & French, J. A. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1469 · Cited by 111 · see citing works
Non-human primate models for investigating fear and anxiety
Barros, M., & Tomaz, C. A. B. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00064-1 · Cited by 109 · see citing works
Stress in early life inhibits neurogenesis in adulthood
Karten, Y. J. G., Olariu, A., & Cameron, H. A. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.01.009 · Cited by 108 · see citing works
(1993) · doi:10.1093/oso/9780198540229.001.0001 · Cited by 105 · see citing works
Behavioral and immunological consequences of brief mother‐infant separation: A species comparison
Laudenslager, M. L., Held, P., Boccia, M. L., Reite, M. L., & Cohen, J. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230305 · Cited by 98 · see citing works
Norcross, J. L., & Newman, J. D. (1999) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1999)47:3 · Cited by 97 · see citing works
Marsden, C. A., King, M. V., & Fone, K. C. F. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.03.003 · Cited by 80 · see citing works
Social buffering of the cortisol response of adult female guinea pigs
Hennessy, M. B., Zate, R., & Maken, D. S. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.12.005 · Cited by 65 · see citing works
Arabadzisz, D., Heijtz, R. D., Knuesel, I., Weber, E., Pilloud, S., Dettling, A. C., Feldon, J., Law, A. J., Harrison, P. J., & Pryce, C. R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.016 · Cited by 60 · see citing works
Corticosterone Peak is Responsible for Stress-Induced Elevation of Glutamate in the Hippocampus
Ábrahám, I. M., Juhász, G. D., Kékesi, K. A., & Kovács, K. (1998) · Stress · doi:10.3109/10253899809167281 · Cited by 59 · see citing works
Marlatt, M. W., Philippens, I. H. C. H. M., Manders, E. M. M., et al. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.05.008 · Cited by 57 · see citing works
Long-term social isolation in the adulthood results in CA1 shrinkage and cognitive impairment
Pereda-Pérez, I., Popović, N., Baño‐Otálora, B., Popović, M., Madrid, J. A., Rol, M. A., & Venero, C. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.07.004 · Cited by 55 · see citing works
Laudenslager, M. L., Boccia, M. L., Berger, C. L., et al. (1995) · Developmental Psychobiology · doi:10.1002/dev.420280402 · Cited by 53 · see citing works
Raminelli, J. L. F., de Sousa, M. B. C., Cunha, M. S., et al. (2001) · Biological Rhythm Research · doi:10.1076/brhm.32.2.159.1357 · Cited by 49 · see citing works
Self-citationAnterior hippocampal volume is reduced in behaviorally depressed female cynomolgus macaques
Willard, S. L., Friedman, D. P., Henkel, C. K., & Shively, C. A. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.04.022 · Cited by 42 · see citing works
Long-term gender behavioral vulnerability after nociceptive neonatal formalin stimulation in rats
Negrigo, A., de Medeiros, M. A., Guinsburg, R., et al. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.12.050 · Cited by 37 · see citing works
Time course of vocal modulation during isolation in common marmosets (Callithrix jacchus)
Yamaguchi, C., Izumi, A., & Nakamura, K. (2010) · American Journal of Primatology · doi:10.1002/ajp.20824 · Cited by 32 · see citing works
Cellular organization of adult neurogenesis in the Common Marmoset
Bunk, E. C., Stelzer, S., Hermann, S., Schäfers, M. A., Schlatt, S., & Schwamborn, J. C. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00639.x · Cited by 32 · see citing works
Lima, M. O., Malheiros, J. M., Negrigo, A., Tescarollo, F. C., de Medeiros, M. A., Suchecki, D., Tannús, A., Guinsburg, R., & Covolan, L. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.10.007 · Cited by 30 · see citing works
Self-citationNeonatal isolation impairs neurogenesis in thedentate gyrus of the guinea pig
Rizzi, S., Bianchi, P., Guidi, S., Ciani, E., & Bartesaghi, R. (2006) · Hippocampus · doi:10.1002/hipo.20247 · Cited by 24 · see citing works
Barbosa, M. N., & Mota, M. T. D. S. (2009) · Primates · doi:10.1007/s10329-009-0137-2 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The effects of social deprivation on adolescent development and mental health
Orben, A., Tomova, L., & Blakemore, S.-J. (2020) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(20)30186-3 · Cited by 1,229 · see citing works
“…in adolescent non-human primates has shown effects in line the rodent research: deprivation of contact with peers for 1-3 weeks results in anxiety-like behaviours and a reduction in cell proliferation and neurogenesis in the hippocampus (a brain region involved in learning and memory)( 57 ).”
Brain-derived neurotrophic factor: a bridge between inflammation and neuroplasticity
Calabrese, F., Rossetti, A. C., Racagni, G., Gass, P., Riva, M. A., & Molteni, R. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00430 · Cited by 482 · see citing works
Links between the neurobiology of oxytocin and human musicality
Harvey, A. R. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.00350 · Cited by 85 · see citing works
Desai, R. I., Limoli, C. L., Stark, C. E. L., & Stark, S. M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104676 · Cited by 55 · see citing works
Unified theory of Alzheimer’s disease (UTAD): implications for prevention and curative therapy
Nehls, M. (2016) · Journal of Molecular Psychiatry · doi:10.1186/s40303-016-0018-8 · Cited by 41 · see citing works
- Authors
- Cinini, S. M., Barnabe, G. F., Galvão-Coelho, N., de Medeiros, M. A., Perez-Mendes, P., Sousa, M. B. C., Covolan, L., & Mello, L. E.
- Affiliations
- Universidade Federal de São Paulo (BR)
- Universidade Federal do Rio Grande do Norte (BR)
- Corresponding author
- Mello, Luiz E.
- Venue
- Frontiers in Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2014-03-27
- Volume
- 8
- Pages
- 45-45
- ISSN
- 1662-453X (ISSN-L)
- PMC
- PMC3973924
- OpenAlex
- W2101446581
- Cited by
- 71
- References
- 61
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 4 · 2023: 2 · 2022: 9 · 2021: 8 · 2020: 10 · 2019: 2 · 2018: 4 · 2017: 10 · 2016: 5 · 2015: 7 · 2014: 1
- FWCI
- 2.67
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- Americanae (AECID Library) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- 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
- social isolation, hippocampal neurogenesis, marmoset, adolescence to adulthood transition, anxiety-like behavior, scent marking, grooming, cortisol, stress, dentate gyrus subgranular zone, neural cell proliferation, doublecortin, BrdU labeling, social deprivation
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
