CHANGES IN STRUCTURAL AND FUNCTIONAL PLASTICITY OF THE BRAIN INDUCED BY ENVIRONMENTAL ENRICHMENT

Cover Page


Cite item

Full Text

Abstract

The review contains current data on structural and functional brain plasticity mechanisms under the enriched environment. Enriched environment contains social and non-social stimuli acting on different aspects of the development and functioning of the brain.  Special attention is devoted to the modeling of enriched environment in the experiment. Enriched environment implies the action of social stimuli, new objects, therefore the enriched environment in animals can be considered as an adequate model to study changes in brain structure and function in people during learning or acquiring complex skills. The review describes the theory of  enriched environment’s influence on neurogenesis, the neuron-glia relationships, and the impact of enriched environment on damaged brain as well as  the possibilities of using the paradigm of enriched environment for neurorehabilitation. Molecular mechanisms of synaptic transmission, which has a correlation with the performance of cognitive functions, are the possible target for the action of environmental factors at the brain under (patho)physiological conditions. The considerable progress has been done in understanding the mechanisms that mediate the effects of  enriched environment on the brain, but still there are many non-resolved questions in the neurochemistry and neurobiology of this phenomenon. Overall, the experience-induced neuroplasticity is a unique mechanism for the development and recovery of brain functions. It opens new perspectives in neuropharmacology and neurorehabilitation.

About the authors

Yu. K. Komleva

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Author for correspondence.
Email: yuliakomleva@mail.ru
PhD student, Department of Biochemistry, with Courses of Medical, Pharmaceutical and Toxicological Chemistry Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 228-07-69 Россия

A. B. Salmina

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Email: allasalmina@mail.ru
PhD, Professor, Head of Department of Biochemistry, with Courses of Medical, Pharmaceutical and Toxicological Chemistry, Vice Rector for Innovative Development and International Activities, Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 2280769 Россия

S. V. Prokopenko

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Email: s.v.proc.58@mail.ru
PhD, Professor, Head of the Department of Nervous Diseases, Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 274-31-74 Россия

L. A. Shestakova

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Email: Patholog-lan@yandex.ru
PhD, Assistant Professor, Head of the Department of Pathological Anatomy named after prof. P.G. Podzolkova, Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 220-14-25 Россия

M. M. Petrova

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Email: stk99@yandex.ru
PhD, Professor, Head of the Polyclinic Therapy Department, Provost for Research, Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 220-06-28 Россия

N. A. Malinovskaya

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Email: reg.kgmu@gmail.com
PhD, Research Worker, Scientific Research Institute of Molecular Medicine and Pathobiochemistry, Assistant Professor, Department of Biochemistry with Courses of the Medical, Pharmaceutical and Toxicological Chemistry, Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 228-07-69 Россия

O. L. Lopatina

Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky, Russian Federation

Email: ol.lopatina@gmail.com
PhD, Senior Lecturer, Department of Biochemistry with Courses of the Medical, Pharmaceutical and Toxicological Chemistry, Krasnoyarsk State Medical University named after prof. V.F. Voyno-Yasenetsky Address: 660022, Krasnoyarsk, Partizana Zheleznyaka St., 1; tel.: (391) 228-07-69 Россия

References

  1. Mayeux R. Epidemiology of neurodegeneration. Ann. Rev. Neurosci. 2003; 26: 81–104.
  2. Nithianantharajah J. Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci. 2006; 7: 697–709.
  3. Nilsson M., Milos P. Enriched environment and astrocytes in central nervous system regeneration. J. Rehabil. Med. 2007; 39: 345–352.
  4. Hummel F.C., Cohen L.G. Drivers of brain plasticity. Curr. Opin. Neurol. 2005; 18: 667–674.
  5. Pascual-Leone A., Amedi A., Fregni F., Merabet L.B. The plastic human brain cortex. Ann. Rev. Neurosci. 2005; 28: 377–401.
  6. Ward N.S., Cohen L.G. Mechanisms underlying recovery of motor function after stroke. Arch. Neurol. 2004; 61: 1844–1848.
  7. Hebb D.O. The effects of early experience on problem-solving at maturity. Am. Psychol. 1947; 2: 306–307.
  8. Will B., Galani R., Kelche C., Rosenzweig M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990–2002). Prog. Neurobiol. 2004; 72: 167–182.
  9. Hubel D.N., Wiesel T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 1970; 206: 419–436.
  10. Rosenzweig M.R., Bennett E.L. Effects of differential environments on brain weights and enzyme activities in gerbils, rats, and mice. Dev. Psychobiol. 1969; 2: 87–95.
  11. Bennett J.C., McRae P.A., Levy L.J., Frick K.M. Long-term continuous, but not daily, environmental enrichment reduces spatial memory decline in aged male mice. Neurobiol. Learn. Mem. 2006; 85: 139–152.
  12. Altman J., Das, G.D. Autoradiographic examination of the effects of enriched environment on the rate of glial multiplication in the adult rat brain. Nature. 1964; 204: 1161–1163.
  13. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 2002; 52: 135–143.
  14. Walsh R.N., Cummins, R.A. Mechanisms mediating the production of environmentally induced brain changes. Psychol. Bull. 1975; 82: 986–1000.
  15. van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 2000; 1: 191–98.
  16. Jankowsky J.L., Melnikova Т., Fadale D.J., Xu G.M., Slunt H.H., Gonzales V., Linda H. Younkin L.H., Steven G., Younkin S.G., Borchelt D.R., Savonenko A.V. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer’s disease. J. Neurosci. 2005; 25: 5217–5224.
  17. Friske J.E., Gammie S.C. Environmental enrichment alters plus maze, but not maternal defense performance in mice. Physiol. Behav. 2005; 85: 187–194.
  18. Lee E.H., Hsu W.L., Ma Y.L., Lee P.J., Chao C.C. Enrichment enhances the expression of sgk, a glucocorticoid-induced gene, and facilitates spatial learning through glutamate AMPA receptor mediation. Eur. J. Neurosci. 2003; 18: 2842–2852.
  19. Meshi D, Drew M.R., Saxe M., Ansorge M.S.; David D., Santarelli L., Malapani C., Moore H., Hen R. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nature Neurosci. 2006; 9: 729–731.
  20. Silva C.F., Duarte F.S., Lima T.C., de Oliveira C.L. Effects of social isolation and enriched environment on behavior of adult Swiss mice do not require hippocampal neurogenesis. Behav. Brain Res. 2011; 225 (1): 85–90.
  21. Johansson B.B., Belichenko P.V. Neuronal plasticity and dendritic spines: effect of environmental enrichment on intact and post-ischemic rat brain. J. Cereb. Blood Flow Metab. 2002; 22: 89–96.
  22. Leggio M.G. Mandolesi L., Federico F., Spirito F., Ricci B., Gelfo F., Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 2005; 163: 78–90.
  23. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., Tsien J.Z., Hu Y. Effects of environmental enrichment on gene expression in the brain. Proc. Natl. Acad. Sci. USA. 2000; 97: 12880–12884.
  24. Rizzi S., Bianchi P., Guidi S., Ciani E., Bartesaghi R. Impact of environmental enrichment on neurogenesis in the dentate gyrus during the early postnatal period. Brain Res. 2011; 1415: 23–33.
  25. Artola A. von Frijtag J.C., Fermont P.C., Gispen W.H., Schrama L.H., Kamal A., Spruijt B.M. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci. 2006; 23: 261–272.
  26. Foster T.C., Dumas T.C. Mechanism for increased hippocampal synaptic strength following differential experience. J. Neurophysiol. 2001; 85: 1377–1383.
  27. Gobbo O.L, O’Mara S.M. Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav. Brain Res. 2004; 152: 231–241.
  28. Lambert T.J., Fernandez S.M., Frick K.M. Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice. Neurobiol. Learn. Mem. 2005; 83: 206–216.
  29. Williamson L.L., Chao A., Bilbo S.D. Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus. Brain Behav. Immun. 2012; 26 (3): 500–510.
  30. Decimo I., Bifari F., Krampera M., Fumagalli G. Neural stem cell niches in health and diseases. Curr. Pharm. Des. 2012; 18 (13): 1755–1783.
  31. Mustroph M.L., Chen S., Desai S.C., Cay E.B., DeYoung E.K., Rhodes J.S. Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience. 2012 6; 219: 62–71.
  32. Schaefers A.T. Rearing conditions and domestication background determine regulation of hippocampal cell proliferation and survival in adulthood - laboratory CD1 and C57Bl/6 mice versus wild house mice. Neuroscience. 2013; 3 (228): 120–127.
  33. Greenough W.T., Hwang H.M., Gorman C. Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc. Natl Acad. Sci. USA. 1985; 82: 4549–4552.
  34. Ickes B.R., Pham T.M., Sanders L.A., Albeck D.S., Mohammed A.H. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol. 2000; 164: 45–52.
  35. Tanti A., Rainer Q., Minier F., Surget A., Belzung C. Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology. 2012; 63 (3): 374–384.
  36. Markham J.A., Greenough W.T. Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol. 2004; 1: 351–363.
  37. Ullian E.M., Sapperstein S.K., Christopherson K.S., Barres B.A. Control of synapse number by glia. Science. 2001; 291: 657–661.
  38. Halassa M.M., Fellin T., Haydon P.G. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 2007; 13: 54–63.
  39. Redolat R., Mesa-Gresa P. Potential benefits and limitations of enriched environments and cognitive activity on age-related behavioural decline. Curr. Top Behav. Neurosci. 2012; 10: 293–316.
  40. Yao Z.H., Zhang J.J., Xie X.F. Enriched environment prevents cognitive impairment and tau hyperphosphorylation after chronic cerebral hypoperfusion. Curr. Neurovasc. Res. 2012; 9 (3): 176–184.
  41. Binder L.I., Guillozet-Bongaarts A.L., Garcia-Sierra F., Berry R.W. Tau, tangles, and Alzheimer’s disease. Biochem. Biophys. Acta. 2005; 1739: 216–223.
  42. Spires T.L., Hyman B.T. Transgenic models of Alzheimer’s disease: learning from animals. NeuroRx. 2005; 2: 423–437.
  43. Coleman P.D., Yao P.J. Synaptic slaughter in Alzheimer’s disease. Neurobiol. Aging. 2003; 24: 1023–1027.
  44. Laurin D., Verreault R., Lindsay J., MacPherson K., Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch. Neurol. 2001; 58: 498–504.
  45. Valenzuela M.J., Sachdev P. Brain reserve and dementia: a systematic review. Psychol. Med. 2006; 36: 441–454.
  46. Wilson R.S. Bennett D.A, Bienias J.L., Aggarwal N.T., Mendes De Leon C.F., Morris M.C., Schneider J.A., Evans D.A. Cognitive activity and incident AD in a population-based sample of older persons. Neurology. 2002; 59: 1910–1914.
  47. Levi O., Jongen-Relo A.L., Feldon J., Roses A.D., Michaelson, D.M. ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol. Dis. 2003; 13: 273–282.
  48. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron. 2003; 37: 925–937.
  49. Walsh D.M, Klyubin I, Fadeeva JV, Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 2002; 416: 535–539.
  50. Fitzjohn S.M., Morton R.A., Kuenzi F., Rosahl T.W., Shearman M., Lewis H., Smith D., Reynolds D.S., Davies C.H., Collingridge G.L., Seabrook G.R. Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J. Neurosci. 2001; 21: 4691–4698.
  51. Prihar G., Verkkoniem A., Perez-Tur J, Crook R., Lincoln S., Houlden H., Somer M., Paetau A., Kalimo H., Grover A., Myllykangas L., Hutton M., Hardy J., Haltia M. Alzheimer disease PS-1 exon 9 deletion defined. Nat Med. 1999; 5: 1090.
  52. Lazarov O., Robinson J., Tang Y.P.,Hairston I.S., Korade-Mirnics Z., Lee V.M., Hersh L.B., Sapolsky R.M., Mirnics K., Sisodia S.S. Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell. 2005; 120: 701–713.
  53. Sheng J.G., Price D.L., Koliatsos V.E. Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of A amyloidosis. J. Neurosci. 2002; 22: 9794–9799.
  54. Brandan E., Inestrosa N.C. Extracellular matrix components and amyloid in neuritic plaques of Alzheimer’s disease. Gen. Pharmacol. 1993; 24: 1063–1068.
  55. Meyer-Luehmann M., Stalder M., Herzig M.C., Kaeser S.A., Kohler E., Pfeifer M., Boncristiano S., Mathews P.M., Mercken M., Abramowski D., Staufenbiel M., Jucker M. Extracellular amyloid formation and associated pathology in neural grafts. Nat. Neurosci. 2003; 6: 370–377.
  56. Iwata H., Mizukami H., Shirotani K., Takaki Y., Muramatsu S., Lu B., Gerard N.P., Gerard C., Ozawa K., Saido T.C. Presynaptic localization of neprilysin contributes to efficient clearance of amyloid-beta peptide in mouse brain. J. Neurosci. 2004; 24: 991–998.
  57. Braun N., Sevigny J., Robson S.C., Enjyoji K., Guckelberger O., Hammer K., Di Virgilio F., Zimmermann H. Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculoture of the brain. Eur. J. Neurosci. 2000; 12: 4357–4366.
  58. Stein T.D., Johnson J.A. Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J. Neurosci. 2002; 22: 7380–7388.
  59. Karsten S.L., Geschwind D.H. Exercise your amyloid. Cell. 2005; 120: 572–574.
  60. Marx J. Preventing Alzheimer’s: a lifelong commitment? J. Neurosci. 2005; 309: 864–866.
  61. Arendash G.W. Garcia M.F., Costa D.A., Cracchiolo J.R., Wefes I.M., Potter H. Environmental enrichment improves cognition in aged Alzheimer’s transgenic mice despite stable β-amyloid deposition. Neuroreport. 2004; 15: 1751–1754.
  62. Adlard P.A., Perreau V.M., Pop V., Cotman C.W. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer’s disease. J. Neurosci. 2005; 25: 4217–4221.
  63. Little D.M., Foxely S., Lazarov O. A preliminary study targeting neuronal pathways activated following environmental enrichment by resting state functional magnetic resonance imaging. J. Alzheimers Dis. 2012; 32 (1): 101–107.
  64. Feng R. Rampon C., Tang Y.P., Shrom D., Jin J., Kyin M., Sopher B., Miller M.W., Ware C.B., Martin G.M., Kim S.H., Langdon R.B., Sisodia S.S., Tsien J.Z. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron. 2001; 32: 911–926.
  65. Wen P.H., Hof P.R., Chen X., Gluck K., Austin G., Younkin S.G., Younkin L.H., DeGasperi R., Gama Sosa M.A., Robakis N.K., Haroutunian V., Elder G.A. The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp. Neurol. 2004; 188: 224–237.
  66. Beauquis J., Pavía P., Pomilio C., Vinuesa A., Podlutskaya N., Galvan V., Saravia F. Environmental enrichment prevents astroglial pathological changes in the hippocampus of APP transgenic mice, model of Alzheimer's disease. Exp. Neurol. 2013; 239: 28–37.
  67. Li S., Jin M, Zhang D., Yang T., Koeglsperger T., Fu H., Selkoe D.J. Environmental novelty activates β2-adrenergic signaling to prevent the impairment of hippocampal LTP by Aβ oligomers. Neuron. 2013; 6, 77 (5): 929–941.
  68. Horner P.J., Gage F.H. Regenerating the damaged nervous system. Nature. 2000; 407: 963–970.
  69. Laviola G., Hannan A.J., Macri S., Solinas M., Jaber M. Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol. Dis. 2008; 31: 159–168.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 1970 "Paediatrician" Publishers LLC



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies