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Experience induces structural and biochemical changes in the adult primate brain

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Kozorovitskiy, Yevgenia, Gross, Charles G., Kopil, Catherine, Battaglia, Lisa, McBreen, Meghan, Stranahan, Alexis M., Gould, Elizabeth·2005·Proceedings of the National Academy of Sciences

Abstract

Primates exhibit complex social and cognitive behavior in the wild. In the laboratory, however, the expression of their behavior is usually limited. A large body of literature shows that living in an enriched environment alters dendrites and synapses in the brains of adult rodents. To date, no studies have investigated the influence of living in a complex environment on brain structure in adult primates. We assessed dendritic architecture, dendritic spines, and synaptic proteins in adult marmosets housed in either a standard laboratory cage or in one of two differentially complex habitats. A month-long stay in either complex environment enhanced the length and complexity of the dendritic tree and increased dendritic spine density and synaptic protein levels in the hippocampus and prefrontal cortex. No differences were detected between the brains of marmosets living in the two differentially complex environments. Our results show that the structure of the adult primate brain remains highly sensitive even to modest levels of experiential complexity. For adult primates, living in standard laboratory housing may induce reversible dendritic spine and synapse decreases in brain regions important for cognition.

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Crossref · 10.1073/pnas.0508817102

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  • The enrichment-induced changes in dendritic complexity, spine density, and synaptic proteins may be a shared feature of resilience under distinct conditions.

    “suggesting that this may be a shared feature of resilience under these two distinct conditions69”

    From Neurobiology of resilience (2012) · cites this paper as [69]

  • Environmental enrichment increases dendritic tree complexity, dendritic spine density, and synaptic protein levels of pyramidal neurons in the hippocampus and prefrontal cortex.

    “environmental enrichment similarly increases the complexity of the dendritic tree, dendritic spine density, and synaptic protein levels of pyramidal neurons in hippocampus and PFC”

    From Neurobiology of resilience (2012) · cites this paper as [69]

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  1. [1]Rosenzweig, M. R., Krech, D., Bennett, E. L. & Diamond, M. C. (1962) J. Comp. Physiol. Psychol. 55, 429-437. [DOI] [PubMed] [Google Scholar]
  2. [2]Walsh, R. N. (1980) Int. J. Neurosci. 11, 77-89. [DOI] [PubMed] [Google Scholar]
  3. [3]Bhide, P. G. & Bedi, K. S. (1984) J. Anat. 138, 447-461. [PMC free article] [PubMed] [Google Scholar]
  4. [6]Diamond, M. C. (2001) An. Acad. Bras. Cienc. 73, 211-220. [DOI] [PubMed] [Google Scholar]
  5. [7]van Praag, H., Kempermann, G. & Gage, F. H. (2000) Nat. Rev. Neurosci. 1, 191-198. [DOI] [PubMed] [Google Scholar]
  6. [8]Holloway, R. L., Jr. (1966) Brain Res. 2, 393-396. [DOI] [PubMed] [Google Scholar]
  7. [9]Mollgaard, K., Diamond, M. C., Bennett, E. L., Rosenzweig, M. R. & Lindner, B. (1971) Int. J. Neurosci. 2, 113-127. [DOI] [PubMed] [Google Scholar]
  8. [10]Globus, A., Rosenzweig, M. R., Bennett, E. L. & Diamond, M. C. (1973) J. Comp. Physiol. Psychol. 82, 175-181. [DOI] [PubMed] [Google Scholar]
  9. [11]Turner, A. M. & Greenough, W. T. (1985) Brain Res. 329, 195-203. [DOI] [PubMed] [Google Scholar]
  10. [12]Camel, J. E., Withers, G. S. & Greenough, W. T. (1986) Behav. Neurosci. 100, 810-813. [DOI] [PubMed] [Google Scholar]
  11. [13]Moser, M. B., Trommald, M. & Andersen, P. (1994) Proc. Natl. Acad. Sci. USA 91, 12673-12675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. [14]Turner, C. A., Lewis, M. H. & King, M. A. (2003) Dev. Psychobiol. 43, 20-27. [DOI] [PubMed] [Google Scholar]
  13. [15]Briones, T. L., Klintsova, A. Y. & Greenough, W. T. (2004) Brain Res. 1018, 130-135. [DOI] [PubMed] [Google Scholar]
  14. [16]Desmond, N. L. & Levy, W. B. (1986) J. Comp. Neurol. 253, 466-475. [DOI] [PubMed] [Google Scholar]
  15. [17]Trommald, M., Hulleberg, G. & Andersen, P. (1996) Learn. Mem. 3, 218-228. [DOI] [PubMed] [Google Scholar]
  16. [18]Kleim, J. A., Swain, R. A., Armstrong, K. A., Napper, R. M., Jones, T. A. & Greenough, W. T. (1998) Neurobiol. Learn. Mem. 69, 274-289. [DOI] [PubMed] [Google Scholar]
  17. [19]Yuste, R. & Bonhoeffer, T. (2001) Annu. Rev. Neurosci. 24, 1071-1089. [DOI] [PubMed] [Google Scholar]
  18. [20]Leuner, B., Falduto, J. & Shors, T. J. (2003) J. Neurosci. 23, 659-665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. [21]Zhou, Q., Homma, K. J. & Poo, M. M. (2004) Neuron 44, 749-757. [DOI] [PubMed] [Google Scholar]
  20. [22]Eadie, B. D., Redila, V. A. & Christie, B. R. (2005) J. Comp. Neurol. 486, 39-47. [DOI] [PubMed] [Google Scholar]
  21. [23]Morris, R. G., Davis, S. & Butcher, S. P. (1990) Philos. Trans. R. Soc. London B 329, 187-204. [DOI] [PubMed] [Google Scholar]
  22. [24]Heynen, A. J., Quinlan, E. M., Bae, D. C. & Bear, M. F. (2000) Neuron 28, 527-536. [DOI] [PubMed] [Google Scholar]
  23. [25]Adams, M. M., Smith, T. D., Moga, D., Gallagher, M., Wang, Y., Wolfe, B. B., Rapp, P. R. & Morrison, J. H. (2001) J. Comp. Neurol. 432, 230-243. [DOI] [PubMed] [Google Scholar]
  24. [26]Nagerl, U. V., Eberhorn, N., Cambridge, S. B. & Bonhoeffer, T. (2004) Neuron 44, 759-767. [DOI] [PubMed] [Google Scholar]
  25. [27]Naka, F., Narita, N., Okado, N. & Narita, M. (2005) Brain Dev. 27, 275-278. [DOI] [PubMed] [Google Scholar]
  26. [28]Struble, R. G. & Riesen, A. H. (1978) Dev. Psychobiol. 11, 479-486. [DOI] [PubMed] [Google Scholar]
  27. [29]Floeter, M. K. & Greenough, W. T. (1979) Science 206, 227-229. [DOI] [PubMed] [Google Scholar]
  28. [30]Bryan, G. K. & Riesen, A. H. (1989) J. Comp. Neurol. 286, 208-217. [DOI] [PubMed] [Google Scholar]
  29. [31]Gabbott, P. L. & Somogyi, J. (1984) J. Neurosci. Methods 11, 221-230. [DOI] [PubMed] [Google Scholar]
  30. [32]Peden, J. K. & von Bonin, G. (1974) J. Comp. Neurol. 86, 37-63. [DOI] [PubMed] [Google Scholar]
  31. [33]Fallon, J. H. & Ziegler, B. T. (1979) Neurosci. Lett. 15, 29-32. [DOI] [PubMed] [Google Scholar]
  32. [34]DeBello, W. M., Feldman, D. E. & Knudsen, E. I. (2001) J. Neurosci. 21, 3161-3174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. [35]Kincaid, A. E., Zheng, T. & Wilson, C. J. (1998) J. Neurosci. 18, 4722-4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. [36]Thiel, G. (1993) Brain Pathol. 3, 87-95. [DOI] [PubMed] [Google Scholar]
  35. [37]Sorra, K. E. & Harris, K. M. (2000) Hippocampus 10, 501-511. [DOI] [PubMed] [Google Scholar]
  36. [38]Bennett, E. L., Krech, D. & Rosenzweig, M. R. (1964) J. Comp. Physiol. Psychol. 57, 440-441. [DOI] [PubMed] [Google Scholar]
  37. [40]Rosenzweig, M. R. (2003) Dev. Neuropsychol. 24, 523-540. [DOI] [PubMed] [Google Scholar]
  38. [41]Kempermann, G., Kuhn, H. G. & Gage, F. H. (1997) Nature 386, 493-495. [DOI] [PubMed] [Google Scholar]
  39. [42]Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O. & Eriksson, P. S. (1999) J. Neurobiol. 39, 569-578. [DOI] [PubMed] [Google Scholar]
  40. [43]Kempermann, G., Gast, D. & Gage, F. H. (2002) Ann. Neurol. 52, 135-143. [DOI] [PubMed] [Google Scholar]
  41. [44]Greenough, W. T., Larson, J. R. & Withers, G. S. (1985) Behav. Neural Biol. 44, 301-314. [DOI] [PubMed] [Google Scholar]
  42. [45]Leuner, B., Mendolia-Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E. & Shors, T. J. (2004) J. Neurosci. 24, 7477-7481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. [46]van Praag, H., Christie, B. R., Sejnowski, T. J. & Gage, F. H. (1999) Proc. Natl. Acad. Sci. USA 96, 13427-13431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. [47]Sackett, G. P. (1972) Neurosci. Res. Prog. Bull. 10, 388-392. [PubMed] [Google Scholar]
  45. [48]Davenport, R. K., Rogers, C. M. & Rumbaugh, D. M. (1973) Dev. Psychol. 9, 343-347. [Google Scholar]
  46. [49]Wilson, M., Warren, J. M. & Abbott, L. (1965) Child Dev. 36, 843-853. [PubMed] [Google Scholar]
  47. [50]Fuller, J. L. & Clark, L. D. (1966) J. Comp. Physiol. Psychol. 61, 258-263. [DOI] [PubMed] [Google Scholar]
  48. [51]Riesen, A. H., Dickerson, G. P. & Struble, R. G. (1977) Ann. N.Y. Acad. Sci. 290, 285-294. [DOI] [PubMed] [Google Scholar]
  49. [52]Rosenzweig, M. R. & Bennett, E. L. (1972) J. Comp. Physiol. Psychol. 80, 304-313. [DOI] [PubMed] [Google Scholar]
  50. [53]Rosenzweig, M. R., Bennett, E. L., Hebert, M. & Morimoto, H. (1978) Brain Res. 153, 563-576. [DOI] [PubMed] [Google Scholar]
  51. [54]Kuenzle, C. C. & Knusel, A. (1974) Physiol. Behav. 13, 205-210. [DOI] [PubMed] [Google Scholar]

Cited by

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Authors
Kozorovitskiy, Y., Gross, C. G., Kopil, C., Battaglia, L., McBreen, M., Stranahan, A. M., & Gould, E.
Affiliations
Princeton University (US)
Venue
Proceedings of the National Academy of Sciences
Published
2005-11-18
Volume
102
Issue
48
Pages
17478-17482
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2141813517
Cited by
202
References
57
Citations by year
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FWCI
3.87
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Institutes of Health
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
environmental enrichment, marmoset, dendritic spine density, dendritic morphology, synaptic proteins, hippocampus, prefrontal cortex, synaptic loss
MeSH terms
Analysis of Variance, Animals, Brain, Callithrix, Carbocyanines, Female, Hydrocortisone, Immunohistochemistry, Male, Nerve Tissue Proteins, Neurons, Social Environment, Synapses, Dendritic Spines

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