Neural consequences of enviromental enrichment
10.1038/35044558
Crossref journal-article
Springer Science and Business Media LLC
Nature Reviews Neuroscience (297)
Bibliography

van Praag, H., Kempermann, G., & Gage, F. H. (2000). Neural consequences of enviromental enrichment. Nature Reviews Neuroscience, 1(3), 191–198.

Authors 3
  1. Henriette van Praag (first)
  2. Gerd Kempermann (additional)
  3. Fred H. Gage (additional)
References 129 Referenced 1,952
  1. Rosenzweig, M. R. in Development and Evolution of Brain Size 263– 293 (Academic Press, 1979). (10.1016/B978-0-12-314650-2.50020-3) / Development and Evolution of Brain Size by MR Rosenzweig (1979)
  2. Renner, M. J. & Rosenzweig, M. R. Enriched and Impoverished Environments: Effects on Brain and Behaviour (Springer, New York, 1987).A comprehensive review of the early literature (1970–80s) on the neuroanatomical, neurochemical and behavioural consequences of enrichment. It also includes the history of enrichment dating back to Charles Darwin. In addition, the generalizability of effects of enrichment across species is reviewed. The authors identify learning as a critical component of the enriched environment. (10.1007/978-1-4612-4766-1) / Enriched and Impoverished Environments: Effects on Brain and Behaviour by MJ Renner (1987)
  3. Hebb, D. O. The Organization of Behaviour (Wiley, New York, 1949 ). / The Organization of Behaviour by DO Hebb (1949)
  4. Hebb, D. O. The effects of early experience on problem-solving at maturity. Am. Psychol. 2, 306–307 (1947). / Am. Psychol. by DO Hebb (1947)
  5. Wiesel, T. N. & Hubel, D. N. Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 28, 1060–1072 (1965). (10.1152/jn.1965.28.6.1060) / J. Neurophysiol. by TN Wiesel (1965)
  6. Hubel, D. N. & Wiesel, T. N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206, 419–436 (1970). (10.1113/jphysiol.1970.sp009022) / J. Physiol. by DN Hubel (1970)
  7. Rosenzweig, M. R. Environmental complexity, cerebral change, and behavior. Am. Psychol. 21, 321–332 ( 1966). (10.1037/h0023555) / Am. Psychol. by MR Rosenzweig (1966)
  8. Rosenzweig, M. R., Krech, D., Bennett, E. L. & Diamond, M. C. Effects of environmental complexity and training on brain chemistry and anatomy . J. Comp. Physiol. Psychol. 55, 429– 437 (1962). (10.1037/h0041137) / J. Comp. Physiol. Psychol. by MR Rosenzweig (1962)
  9. Rosenzweig, M. R. & Bennett, E. L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 78, 57–65 (1996). (10.1016/0166-4328(95)00216-2) / Behav. Brain Res. by MR Rosenzweig (1996)
  10. Rosenzweig, M. R. & Bennett, E. L. Effects of differential environments on brain weights and enzyme activities in gerbils, rats, and mice. Dev. Psychobiol. 2, 87– 95 (1969). (10.1002/dev.420020208) / Dev. Psychobiol. by MR Rosenzweig (1969)
  11. Rosenzweig, M. R., Bennett, E. L. & Diamond, M. C. in Psychopathology of Mental Development. (eds Zubin, J. & Jervis, G.) 45–56 (Grune & Stratton, New York, 1967). / Psychopathology of Mental Development by MR Rosenzweig (1967)
  12. Bennett, E. L., Rosenzweig, M. R. & Diamond, M. C. Rat brain: effects of environmental enrichment on wet and dry weights. Science 164, 825– 826 (1969). (10.1126/science.163.3869.825) / Science by EL Bennett (1969)
  13. Bennett, E. L. in Neural Mechanisms of Learning and Memory (eds Rosenzweig, M. R. & Bennett, E. L) 279–287 (MIT Press, Cambridge, Massachusetts, 1976). / Neural Mechanisms of Learning and Memory by EL Bennett (1976)
  14. Cummins, R. A., Walsh, R., Budtz-Olsen, O. E., Konstantinos, T. & Horsfall, C. R. Environmentally-induced changes in the brains of elderly rats. Nature 243, 516–518 (1973). (10.1038/243516a0) / Nature by RA Cummins (1973)
  15. Holloway, R. L. Dendritic branching: some preliminary results of training and complexity in rat visual cortex. Brain Res. 2, 393– 396 (1966). (10.1016/0006-8993(66)90009-6) / Brain Res. by RL Holloway (1966)
  16. Diamond, M. C. et al. Increases in cortical depth and glia numbers in rats subjected to enriched environment. J. Comp. Neurol. 128, 117–126 (1966). (10.1002/cne.901280110) / J. Comp. Neurol. by MC Diamond (1966)
  17. Diamond, M. C., Ingham, C. C., Johnson, R. E., Bennett, E. L. & Rosenzweig, M. R. Effects of environment on morphology of rat cerebral cortex and hippocampus. J. Neurobiol. 7, 75–85 (1976 ). (10.1002/neu.480070108) / J. Neurobiol. by MC Diamond (1976)
  18. Greenough, W. T. & Volkmar, F. R. Pattern of dendritic branching in occipital cortex of rats reared in complex environments . Exp. Neurol. 40, 491– 504 (1973). (10.1016/0014-4886(73)90090-3) / Exp. Neurol. by WT Greenough (1973)
  19. Greenough, W. T. Neural Mechanisms of Learning and Memory (eds Rosenzweig, M. R. & Bennett, E. L.) 255–278 (MIT Press, Cambridge, Massachusetts, 1976).Discusses similarities between enrichment and learning on brain and behaviour. In addition, changes in synaptic size and dendritic branching in response to enrichment are reviewed in detail. / Neural Mechanisms of Learning and Memory by WT Greenough (1976)
  20. Greenough, W. T., West, R. W. & DeVoogd, T. J. Postsynaptic plate perforations: changes with age and experience in the rat. Science 202, 1096–1098 (1978). (10.1126/science.715459) / Science by WT Greenough (1978)
  21. Walsh, R. N., Budtz-Olsen, O. E., Penny, J. E. & Cummins, R. A. The effects of environmental complexity on the histology of the rat hippocampus . J. Comp. Neurol. 137, 361– 366 (1969). (10.1002/cne.901370309) / J. Comp. Neurol. by RN Walsh (1969)
  22. Walsh, R. N. & Cummins, R. A. Changes in hippocampal neuronal nuclei in response to environmental stimulation. Int. J. Neurosci. 9, 209–212 ( 1979). (10.3109/00207457909147675) / Int. J. Neurosci. by RN Walsh (1979)
  23. 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 204, 1161– 1163 (1964).Investigated whether enrichment could add new neurons to the adult brain. The focus of the paper was on cortex rather than hippocampus and no new neurons were observed in response to environmental changes. Subsequent studies focused on structural changes in existing cells in response to enrichment. (10.1038/2041161a0) / Nature by J Altman (1964)
  24. Kempermann, G., Kuhn, H. G. & Gage, F. H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493– 495 (1997).The first paper to show that enrichment increases the survival of newborn cells in the dentate gyrus of the hippocampus in adult mice. Enriched mice had 57% more BrdU-positive cells per dentate gyrus than controls. Cell proliferation, however, was not affected. (10.1038/386493a0) / Nature by G Kempermann (1997)
  25. Rosenzweig, M. R., Bennett, E. L., Hebert, M. & Morimoto, H. Social grouping cannot account for cerebral effects of enriched environments . Brain Res. 153, 563–576 (1978). (10.1016/0006-8993(78)90340-2) / Brain Res. by MR Rosenzweig (1978)
  26. Bernstein, L. A study of some enriching variables in a free-environment for rats. J. Psychosomatic Res. 17, 85–88, (1973). (10.1016/0022-3999(73)90008-1) / J. Psychosomatic Res. by L Bernstein (1973)
  27. Ferchmin, P. A. & Bennett, E. L. Direct contact with enriched environment is required to alter cerebral weights in rats. J. Comp. Physiol. Psychol. 88, 360– 367 (1975). (10.1037/h0076175) / J. Comp. Physiol. Psychol. by PA Ferchmin (1975)
  28. Walsh, R. N. & Cummins, R. A. Mechanisms mediating the production of environmentally induced brain changes. Psychol. Bull. 82, 986–1000 (1975). (10.1037/0033-2909.82.6.986) / Psychol. Bull. by RN Walsh (1975)
  29. Van Praag, H., Kempermann, G. & Gage, F. H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neurosci. 2, 266–270 (1999). Studied the effects of components of the enriched environment such as learning and motor activity on neurogenesis. No effect of learning was observed. However, this is the first study to show that voluntary activity on a wheel increases cell proliferation and survival in the dentate gyrus. (10.1038/6368) / Nature Neurosci. by H Van Praag (1999)
  30. Ambrogini, P. et al. Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci. Lett. 286, 21–24 (2000). (10.1016/S0304-3940(00)01074-0) / Neurosci. Lett. by P Ambrogini (2000)
  31. Gould, E. et al. Learning enhances adult neurogenesis in the hippocampal formation . Nature Neurosci. 2, 260– 265 (1999). (10.1038/6365) / Nature Neurosci. by E Gould (1999)
  32. Greenough, W. T., Cohen, N. J. & Juraska, J. M. New neurons in old brains: learning to survive? Nature Neurosci. 2, 203–205 (1999). (10.1038/6300) / Nature Neurosci. by WT Greenough (1999)
  33. Lemaire, V., Koehl, M., Le Moal, M. & Abrous, D. N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl Acad. Sci. USA 97, 11032–11037 (2000). (10.1073/pnas.97.20.11032) / Proc. Natl Acad. Sci. USA by V Lemaire (2000)
  34. Pacteau, C., Einon, D. & Sinden, J. Early rearing environment and dorsal hippocampal ibotenic acid lesions: long-term influences on spatial learning and alternation in the rat. Behav. Brain Res. 34, 79– 96 (1989). (10.1016/S0166-4328(89)80092-0) / Behav. Brain Res. by C Pacteau (1989)
  35. Wainwright, P. E. et al. Effects of environmental enrichment on cortical depth and Morris-maze performance in B6D2F2 mice exposed prenatally to ethanol. Neurotoxicol. Teratol. 15, 11–20 (1993). (10.1016/0892-0362(93)90040-U) / Neurotoxicol. Teratol. by PE Wainwright (1993)
  36. Kempermann, G., Kuhn, H. G. & Gage, F. H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206– 3212 (1998). (10.1523/JNEUROSCI.18-09-03206.1998) / J. Neurosci. by G Kempermann (1998)
  37. Fordyce, D. E. & Farrar, R. P. Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav. Brain Res. 46, 123–133 (1991). (10.1016/S0166-4328(05)80105-6) / Behav. Brain Res. by DE Fordyce (1991)
  38. Fordyce, D. E. & Wehner, J. M. Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Res. 619, 111–119 ( 1993). (10.1016/0006-8993(93)91602-O) / Brain Res. by DE Fordyce (1993)
  39. Van Praag, H., Christie, B. R., Sejnowski, T. J. & Gage, F. H. Running enhances neurogenesis, learning and long-term potentiation in mice . Proc. Natl Acad. Sci. USA 96, 13427– 13431 (1999). (10.1073/pnas.96.23.13427) / Proc. Natl Acad. Sci. USA by H Van Praag (1999)
  40. Altman, J. Are new neurons formed in the brains of adult mammals? Science 135, 1127–1128 ( 1962). (10.1126/science.135.3509.1127) / Science by J Altman (1962)
  41. Szeligo, F. & Leblond, C. P. Response of three main types of glial cells of cortex and corpus callosum in rats handled during suckling or exposed to enriched, control, or impoverished environments following weaning . J. Comp. Neurol. 172, 247– 264 (1977). (10.1002/cne.901720205) / J. Comp. Neurol. by F Szeligo (1977)
  42. Kempermann, G., Kuhn, H. G. & Gage, F. H. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc. Natl Acad. Sci. USA 94, 10409–10414 (1997). (10.1073/pnas.94.19.10409) / Proc. Natl Acad. Sci. USA by G Kempermann (1997)
  43. Kempermann, G., Brandon, E. P. & Gage, F. H. Environmental stimulation of 129/SvJ mice results in increased cell proliferation and neurogenesis in the adult dentate gyrus . Curr. Biol. 8, 939–942 (1998). (10.1016/S0960-9822(07)00377-6) / Curr. Biol. by G Kempermann (1998)
  44. Altman, J., Wallace, R. B., Anderson, W. J. & Das, G. D. Behaviorally induced changes in length of cerebrum in rat. Dev. Psychobiol. 1, 112–117 ( 1968). (10.1002/dev.420010209) / Dev. Psychobiol. by J Altman (1968)
  45. Diamond, M. C., Lindner, B. & Raymond, A. Extensive cortical depth measurements and neuron size increases in the cortex of environmentally enriched rats. J. Comp. Neurol. 131, 357–364 ( 1967). (10.1002/cne.901310305) / J. Comp. Neurol. by MC Diamond (1967)
  46. Volkmar, F. R. & Greenough, W. T. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176, 1445–1447 ( 1972). (10.1126/science.176.4042.1445) / Science by FR Volkmar (1972)
  47. Globus, A., Rosenzweig, M. R., Bennett, E. L. & Diamond, M. C. Effects of differential environments on dendritic spine counts. J. Comp. Phys. Psych. 84, 598–604 (1973). (10.1037/h0034880) / J. Comp. Phys. Psych. by A Globus (1973)
  48. Bhide, P. G. & Bedi, K. S. The effects of a lengthy period of environmental diversity of well-fed and previously undernourished rats. II. Synapse to neurons ratios. J. Comp. Neurol. 227 , 305–310 (1984). (10.1002/cne.902270213) / J. Comp. Neurol. by PG Bhide (1984)
  49. Beaulieu, C. & Colonnier, M. The effect of richness of the environment on cat visual cortex. J. Comp. Neurol. 266, 478–494 (1987). (10.1002/cne.902660404) / J. Comp. Neurol. by C Beaulieu (1987)
  50. Juraska, J. M., Fitch, J. M., Henderson, C. & Rivers, N. Sex differences in the dendritic branching of dentate granule cells following differential experience. Brain Res. 333, 73–80 (1985). (10.1016/0006-8993(85)90125-8) / Brain Res. by JM Juraska (1985)
  51. Altschuler, R. A. Morphometry of the effect of increased experience and training on synaptic density in area CA3 of the rat hippocampus. J. Histochem. Cytochem. 27, 1548–1550 ( 1979). (10.1177/27.11.512348) / J. Histochem. Cytochem. by RA Altschuler (1979)
  52. Rampon, C. et al. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nature Neurosci. 3, 205–206 (2000). (10.1038/72945) / Nature Neurosci. by C Rampon (2000)
  53. Kleim, J. A., Lussnig, E., Schwarz, E. R., Comery, T. A. & Greenough, W. T. Synaptogenesis and FOS expression in the motor cortex of the adult rat after motor skill learning . J. Neurosci. 16, 4529– 4535 (1996). (10.1523/JNEUROSCI.16-14-04529.1996) / J. Neurosci. by JA Kleim (1996)
  54. Black, J. E. Isaacs, K. R., Anderson, B. J., Alcantara, A. A. & Greenough, W. T. Leaning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl Acad. Sci. USA 87, 5568–5572 (1990). (10.1073/pnas.87.14.5568) / Proc. Natl Acad. Sci. USA by JE Black (1990)
  55. Isaacs, K. R., Anderson, B. J., Alcantara, A. A., Black, J. E. & Greenough, W. T. Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J. Cereb. Blood Flow Metab. 12, 110–119 (1992). (10.1038/jcbfm.1992.14) / J. Cereb. Blood Flow Metab. by KR Isaacs (1992)
  56. Green, E. J. & Greenough, W. T. Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro. J. Neurophysiol. 55, 739–750 (1986). (10.1152/jn.1986.55.4.739) / J. Neurophysiol. by EJ Green (1986)
  57. Foster, T. C., Fugger, H. N. & Cunningham, S. G. Receptor blockade reveals a correspondence between hippocampal-dependent behavior and experience-dependent synaptic enhancement . Brain Res. 871, 39–43 (2000). (10.1016/S0006-8993(00)02379-9) / Brain Res. by TC Foster (2000)
  58. Sharp, P. E., McNaughton, B. L. & Barnes, C. A. Enhancement of hippocampal field potentials in rats exposed to a novel, complex environment. Brain Res. 339, 361–365 (1985). (10.1016/0006-8993(85)90105-2) / Brain Res. by PE Sharp (1985)
  59. Vanderwolf, C. H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407– 418 (1969). (10.1016/0013-4694(69)90092-3) / Electroencephalogr. Clin. Neurophysiol. by CH Vanderwolf (1969)
  60. Czurko, A., Hirase, H., Csicsvari, J. & Buzsaki, G. Sustained activation of hippocampal pyramidal cells by 'space clamping' in a running wheel. Eur. J. Neurosci. 11, 344 –352 (1999). (10.1046/j.1460-9568.1999.00446.x) / Eur. J. Neurosci. by A Czurko (1999)
  61. Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 , 31–39 (1993). (10.1038/361031a0) / Nature by TV Bliss (1993)
  62. Bronzino, J. D. et al. Maturation of long-term potentiation in the hippocampal dentate gyrus of the freely moving rat. Hippocampus 4, 439–446 (1994). (10.1002/hipo.450040406) / Hippocampus by JD Bronzino (1994)
  63. Wang, S., Scott, B. W. & Wojtowicz, J. M. Heterogenous properties of dentate granule neurons in adult rat. J. Neurobiol. 42, 248– 257 (2000). (10.1002/(SICI)1097-4695(20000205)42:2<248::AID-NEU8>3.0.CO;2-J) / J. Neurobiol. by S Wang (2000)
  64. Calof, A. L. Intrinsic and extrinsic factors regulating vertebrate neurogenesis. Curr. Opin. Neurobiol. 5, 19–27 (1995). (10.1016/0959-4388(95)80082-4) / Curr. Opin. Neurobiol. by AL Calof (1995)
  65. Aberg, M. A. I. et al. Peripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 20, 2896–2903 (2000). (10.1523/JNEUROSCI.20-08-02896.2000) / J. Neurosci. by MAI Aberg (2000)
  66. Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J. & Gage, F. H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17, 5820– 5829 (1997). (10.1523/JNEUROSCI.17-15-05820.1997) / J. Neurosci. by HG Kuhn (1997)
  67. Wagner, J. P., Black, I. B. & DiCicco-Bloom, E. Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J. Neurosci. 19, 6006–6016 (1999). (10.1523/JNEUROSCI.19-14-06006.1999) / J. Neurosci. by JP Wagner (1999)
  68. Rasika, S., Alvarez-Buylla, A. & Nottebohm, F. BDNF mediates the effects of testosterone on the survial of new neurons in an adult brain. Neuron 22, 53–62 (1999). (10.1016/S0896-6273(00)80678-9) / Neuron by S Rasika (1999)
  69. Mohammed, A. H. et al. Environmental influences on the central nervous system and their implications for the aging rat. J. Brain Res. 57, 183–191 (1993). / J. Brain Res. by AH Mohammed (1993)
  70. Pham, T. M. et al. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year . Neuroscience 94, 279– 286 (1999). (10.1016/S0306-4522(99)00316-4) / Neuroscience by TM Pham (1999)
  71. Falkenberg, T. et al. Increased expression of brain-derived neurotrophic factor mRNA in rat is associated with improved spatial memory and enriched environment . Neurosci. Lett. 138, 153– 156 (1992). (10.1016/0304-3940(92)90494-R) / Neurosci. Lett. by T Falkenberg (1992)
  72. Young, D. et al. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nature Med. 5, 448–453 (1999). (10.1038/7449) / Nature Med. by D Young (1999)
  73. Carro, E. et al. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 20, 2926–2933 (2000). (10.1523/JNEUROSCI.20-08-02926.2000) / J. Neurosci. by E Carro (2000)
  74. Gomez-Pinilla, F., Dao, L. & Vannarith, S. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res. 764, 1– 8 (1997). (10.1016/S0006-8993(97)00375-2) / Brain Res. by F Gomez-Pinilla (1997)
  75. Gomez-Pinilla, F., So, V. & Kesslak, J. P. Spatial learning and physical activity contribute to the induction of fibroblast growth factor: neural substrates for increased cognition associated with exercise. Neuroscience 85, 53–61 (1998). (10.1016/S0306-4522(97)00576-9) / Neuroscience by F Gomez-Pinilla (1998)
  76. Neeper, S. A., Gomez-Pinilla, F., Choi, J. & Cotman, C. Exercise and brain neurotrophins. Nature 373, 109 (1995).The first paper to indicate that growth factors may mediate the beneficial effects of exercise on the brain. Specifically, voluntary exercise in rats increased levels of BDNF mRNA in hippocampus and cortex. (10.1038/373109a0) / Nature by SA Neeper (1995)
  77. Widenfalk, J., Olson, L. & Thoren, P. Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain. Neurosci. Res. 34, 125–132 (1999). (10.1016/S0168-0102(99)00051-6) / Neurosci. Res. by J Widenfalk (1999)
  78. Kang, H. & Schuman, E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658–1662 ( 1995). (10.1126/science.7886457) / Science by H Kang (1995)
  79. Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T. & Lu, B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706–709 ( 1996). (10.1038/381706a0) / Nature by A Figurov (1996)
  80. Fischer, W. et al. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329, 65–68 (1987). (10.1038/329065a0) / Nature by W Fischer (1987)
  81. Por, S. B., Bennett, E. L. & Bondy, S. C. Environmental enrichment and neurotransmitter receptors . Behav. Neural Biol. 34, 132– 140 (1982). (10.1016/S0163-1047(82)91514-X) / Behav. Neural Biol. by SB Por (1982)
  82. Rasmuson, S. et al. Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Brain Res. Mol Brain Res. 53, 285–290 (1998). (10.1016/S0169-328X(97)00317-3) / Brain Res. Mol Brain Res. by S Rasmuson (1998)
  83. Krech, D., Rosenzweig, M. R. & Bennet, E. L. Effects of environmental complexity and training on brain chemistry. J. Comp. Physiol. Psychol. 53, 509–515 (1960). (10.1037/h0045402) / J. Comp. Physiol. Psychol. by D Krech (1960)
  84. Zolman, J. & Morimoto, H. Cerebral changes related to duration of environmental complexity and locomotor activity. J. Comp. Physiol. Psychol. 60, 382–387 ( 1965). (10.1037/h0022547) / J. Comp. Physiol. Psychol. by J Zolman (1965)
  85. Fordyce, D. E. & Farrar, R. P. Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav. Brain Res. 43, 115–123 (1991). (10.1016/S0166-4328(05)80061-0) / Behav. Brain Res. by DE Fordyce (1991)
  86. Sforzo, G. A., Seeger, T. F., Pert, C. B., Pert, A. & Dotson, C. O. In vivo opioid receptor occupation in the rat brain following exercise. Med. Sci. Sports Exerc. 18, 380–384 ( 1986). (10.1249/00005768-198608000-00003) / Med. Sci. Sports Exerc. by GA Sforzo (1986)
  87. Soares, J. et al. Brain noradrenergic responses to footshock after chronic activity-wheel running. Behav. Neurosci. 113, 558– 566 (1999). (10.1037/0735-7044.113.3.558) / Behav. Neurosci. by J Soares (1999)
  88. Chaouloff, F. Physical exercise and brain monoamines: a review. Acta Physiol. Scand. 137, 1–13 ( 1989). (10.1111/j.1748-1716.1989.tb08715.x) / Acta Physiol. Scand. by F Chaouloff (1989)
  89. Dawirs, R. R., Hildebrandt, K. & Teuchert-Noodt, G. Adult treatment with haloperidol increases dentate granule cell proliferation in the gerbil hippocampus. J. Neural Transm. 105, 317–327 (1998). (10.1007/s007020050061) / J. Neural Transm. by RR Dawirs (1998)
  90. Malberg, J. E. et al. Chronic antidepressant administration increases granule cell genesis in the hippocampus of the adult male rat. J. Neurosci. (in the press).
  91. Madsen T. M. et al. Increased neurogenesis in a model of electroconvulsive therapy . Biol. Psychiatry 47, 1043– 1049 (2000). (10.1016/S0006-3223(00)00228-6) / Biol. Psychiatry by TM Madsen (2000)
  92. Brezun, J. M. & Daszuta, A. Serotonergic reinnervation reverses lesion-induced decreases in PSA-NCAM labeling and proliferation of hippocampal cells in adult rats. Hippocampus 10, 37– 46 (2000). (10.1002/(SICI)1098-1063(2000)10:1<37::AID-HIPO4>3.0.CO;2-C) / Hippocampus by JM Brezun (2000)
  93. Brezun, J. M. & Daszuta, A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats . Neuroscience 89, 999– 1002 (1999). (10.1016/S0306-4522(98)00693-9) / Neuroscience by JM Brezun (1999)
  94. Will, B. E., Rosenzweig, M. R., Bennett, E. L., Hebert, M. & Morimoto, H. A relatively brief environmental enrichment aids recovery of learning capacity and alters brain measures after postweaning brain lesions in rats. J. Comp. Physiol. Psych. 91, 33–50 (1977). An important study of the effects of enrichment on recovery from brain lesions. Issues related to the age of the animal at time of injury and the amount of enrichment needed for therapeutic purposes were investigated. The authors found that enrichment of two hours a day was as beneficial as 24 hours a day. (10.1037/h0077306) / J. Comp. Physiol. Psych. by BE Will (1977)
  95. Darymple-Alford, J. C. & Benton, D. Preoperative differential housing and dorsal hippocampal lesions in rats. Behav. Neurosci. 98, 23–34 ( 1984). (10.1037/0735-7044.98.1.23) / Behav. Neurosci. by JC Darymple-Alford (1984)
  96. Gentile, A. M. & Beheshti, Z. Enrichment versus exercise effects on motor impairments following cortical removals in rats . Behav. Neural Biol. 47, 321– 332 (1987). (10.1016/S0163-1047(87)90435-3) / Behav. Neural Biol. by AM Gentile (1987)
  97. Johansson, B. B. Functional outcome in rats transferred to an enriched environment 15 days after focal brain ischemia. Stroke 27, 324 –326 (1996). (10.1161/01.STR.27.2.324) / Stroke by BB Johansson (1996)
  98. Stummer, W., Weber, K., Tranmer, B., Baethmann, A. & Kempski, O. Reduced mortality and brain damage after locomotor activity in gerbil forebrain ischemia. Stroke 25, 1862–1869 (1994). (10.1161/01.STR.25.9.1862) / Stroke by W Stummer (1994)
  99. Stummer, W., Baethmann, A., Murr, R., Schurere, L. & Kempski, O. S. Cerebral protection against ischemia by locomotor activity in gerbils: underlying mechanisms. Stroke 26, 1423–1430 (1995). (10.1161/01.STR.26.8.1423) / Stroke by W Stummer (1995)
  100. Johansson, B. B. & Ohlsson, A. Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat. Exp. Neurol. 139, 322–327 (1996). (10.1006/exnr.1996.0106) / Exp. Neurol. by BB Johansson (1996)
  101. van Dellen, A., Blakemore, C., Deacon, R., York, D. & Hannan, A. J. Delaying the onset of Huntington's in mice. Nature 404, 721– 722 (2000). (10.1038/35008142) / Nature by A van Dellen (2000)
  102. Gerlai, R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 19, 177– 181 (1996). (10.1016/S0166-2236(96)20020-7) / Trends Neurosci. by R Gerlai (1996)
  103. Bennet, E. L. et al. Effects of successive environments on brain measures. Physiol. Behav. 12, 621–631 (1974). (10.1016/0031-9384(74)90212-1) / Physiol. Behav. by EL Bennet (1974)
  104. Kempermann, G. & Gage, F. H. Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 9, 321–332 (1999). (10.1002/(SICI)1098-1063(1999)9:3<321::AID-HIPO11>3.0.CO;2-C) / Hippocampus by G Kempermann (1999)
  105. Brasted, P. J., Watts, C., Robbins, T. W. & Dunnett, S. B. Associative plasticity in striatal transplants. Proc. Natl Acad. Sci. USA 96, 10524–10529 (1999). (10.1073/pnas.96.18.10524) / Proc. Natl Acad. Sci. USA by PJ Brasted (1999)
  106. Belanger, M., Drew, T., Provencher, J. & Rossilong, S. A comparison of locomotion in adult cats before and after spinal transection. J. Neurophys. 76, 471–491 (1996). (10.1152/jn.1996.76.1.471) / J. Neurophys. by M Belanger (1996)
  107. de Leon, R. D., Hodgson, J. A., Roy, R. R. & Edgerton, V. R. Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J. Neurophysiol. 81, 85 –94 (1999). (10.1152/jn.1999.81.1.85) / J. Neurophysiol. by RD de Leon (1999)
  108. Horner, P. J. & Gage, F. H. Regenerating the damaged nervous system. Nature 407, 963– 970 (2000). (10.1038/35039559) / Nature by PJ Horner (2000)
  109. Barnea, A. & Nottebohm, F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl Acad. Sci. USA 91, 11217–11221 (1994).Suggests a correlation between neurogenesis and the formation of new memories in birds. Subsequent work in mammals has supported this hypothesis. (10.1073/pnas.91.23.11217) / Proc. Natl Acad. Sci. USA by A Barnea (1994)
  110. Barnea, A. & Nottebohm, F. Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc. Natl Acad. Sci. USA 93, 714–718 (1996). (10.1073/pnas.93.2.714) / Proc. Natl Acad. Sci. USA by A Barnea (1996)
  111. Levine, S. Infantile experience and resistance to physiological stress. Science 126, 405–406 ( 1957). (10.1126/science.126.3270.405) / Science by S Levine (1957)
  112. Meaney, M. J., Aitken, D. H., van Berkel, C., Bhatnagar, S. & Sapolsky, R. M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239, 766–768 ( 1988). (10.1126/science.3340858) / Science by MJ Meaney (1988)
  113. Meaney, M. J. et al. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology 16 , 85–103 (1991). (10.1016/0306-4530(91)90072-2) / Psychoneuroendocrinology by MJ Meaney (1991)
  114. Francis, D. D. & Meaney, M. J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 9, 128–134 ( 1999). (10.1016/S0959-4388(99)80016-6) / Curr. Opin. Neurobiol. by DD Francis (1999)
  115. Liu, D., Diorio, J., Day, J. C., Francis, D. D. & Meaney, M. J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neurosci. 3, 799–806 (2000). (10.1038/77702) / Nature Neurosci. by D Liu (2000)
  116. Kuhn, C. M., Butler, S. R. & Schanberg, S. M. Selective depression of serum growth hormone during maternal deprivation in rat pups. Science 201, 1034–1036 (1978). (10.1126/science.684424) / Science by CM Kuhn (1978)
  117. Plotsky, P. M. & Meaney, M. J. Early postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in rats. Mol. Brain Res. 18, 195–200 (1993). (10.1016/0169-328X(93)90189-V) / Mol. Brain Res. by PM Plotsky (1993)
  118. Oitzl, M. S., Workel, J. O., Fluttert, M., Frosch, F. & DeKloet, E. R. Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur. J. Neurosci. 12, 3771–3780 (2000). (10.1046/j.1460-9568.2000.00231.x) / Eur. J. Neurosci. by MS Oitzl (2000)
  119. Hofer, M. A. On the nature and consequences of early loss. Psychosomatic Med. 58, 570–581 ( 1996). (10.1097/00006842-199611000-00005) / Psychosomatic Med. by MA Hofer (1996)
  120. Hamm, R. J. Temple, M. D., O'Dell, D. M., Pike, B. R. & Lyeth, B. G. Exposure to environmental complexity promotes recovery of cognitive function after traumatic brain injury. J. Neurotrauma 13, 41–47 (1996). (10.1089/neu.1996.13.41) / J. Neurotrauma by RJ Hamm (1996)
  121. Kolb, B. & Gibb, R. Environmental enrichment and cortical injury: behavioral and anatomical consequences of frontal cortex lesions. Cereb. Cortex 1, 189–198 (1991). (10.1093/cercor/1.2.189) / Cereb. Cortex by B Kolb (1991)
  122. Dahlqvist, P. et al. Environmental enrichment alters nerve growth factor-induced gene A and glucocorticoid receptor messenger RNA expression after middle cerebral artery occlusion in rats. Neuroscience 93, 527–535 (1999). (10.1016/S0306-4522(99)00183-9) / Neuroscience by P Dahlqvist (1999)
  123. Zhao, L. R., Mattsson, B. & Johansson, B. B. Environmental influence on brain-derived neurotrophic factor messenger RNA expression after middle cerebral artery occlusion in spontaneously hypertensive rats. Neuroscience 97, 177–184 (2000). (10.1016/S0306-4522(00)00023-3) / Neuroscience by LR Zhao (2000)
  124. Soffie, M., Hahn, K., Terao, E. & Eclancher, F. Behavioural and glial changes in old rats following environmental enrichment. Behav. Brain Res. 101, 37–49 (1999). (10.1016/S0166-4328(98)00139-9) / Behav. Brain Res. by M Soffie (1999)
  125. Winocur, G. Environmental influences on cognitive decline in aged rats. Neurobiol. Aging 19, 589–597 ( 1998). (10.1016/S0197-4580(98)00107-9) / Neurobiol. Aging by G Winocur (1998)
  126. Nakamura, H., Kobayashi, S., Ohashi, Y. & Ando, S. Age-changes of brain synapses and synaptic plasticity in response to an enriched environment . J. Neurosci. Res. 56, 307– 315 (1999). (10.1002/(SICI)1097-4547(19990501)56:3<307::AID-JNR10>3.0.CO;2-3) / J. Neurosci. Res. by H Nakamura (1999)
  127. Widman, D. R., Abrahamsen, G. C. & Rosellini, R. A. Environmental enrichment: the influences of restricted daily exposure and subsequent exposure to uncontrollable stress. Physiol. Behav. 51, 309–318 (1992). (10.1016/0031-9384(92)90146-S) / Physiol. Behav. by DR Widman (1992)
  128. Rema, V. & Ebner, F. F. Effect of enriched environment rearing on impairments in cortical excitability and plasticity after prenatal alcohol exposure. J. Neurosci. 19, 10993 –11006 (1999). (10.1523/JNEUROSCI.19-24-10993.1999) / J. Neurosci. by V Rema (1999)
  129. Warren, J. M., Zerweck, C. & Anthony, A. Effects of environmental enrichment on old mice. Dev. Psychobiol. 15, 13–18 (1982). (10.1002/dev.420150104) / Dev. Psychobiol. by JM Warren (1982)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 4:48 a.m.)
Deposited 2 years, 3 months ago (May 16, 2023, 10:15 p.m.)
Indexed 19 minutes ago (Aug. 29, 2025, 10:38 a.m.)
Issued 24 years, 8 months ago (Dec. 1, 2000)
Published 24 years, 8 months ago (Dec. 1, 2000)
Published Print 24 years, 8 months ago (Dec. 1, 2000)
Funders 0

None

@article{van_Praag_2000, title={Neural consequences of enviromental enrichment}, volume={1}, ISSN={1471-0048}, url={http://dx.doi.org/10.1038/35044558}, DOI={10.1038/35044558}, number={3}, journal={Nature Reviews Neuroscience}, publisher={Springer Science and Business Media LLC}, author={van Praag, Henriette and Kempermann, Gerd and Gage, Fred H.}, year={2000}, month=dec, pages={191–198} }