In the present paper, we focus on neuronal changes that occur in response to complex stimulation by an enriched environment. An enriched environment is 'enriched' in relation to standard laboratory housing conditions. In general the 'enriched' animals are kept in larger cages and in larger groups with tunnels, nesting material and toys.
Exposure to an enriched environment has been found to elicit neuroanatomical and behavioural changes, such as enhanced dendritic arborization, gliogenesis, neurogenesis, and improved learning.
It is difficult to isolate the behavioural factors that are responsible for neural changes. Factors such as social interaction, learning and motor activity have been suggested to mediate neural consequences of the enriched environment.
Similar to the effects of environmental enrichment, voluntary exercise in a running wheel enhances the survival of newborn neurons in the dentate gyrus. In addition, both conditions improve learning and memory. Therefore effects of enrichment and exercise on behavioural, morphological and molecular changes in the brain are compared in the review.
Enrichment increases dendritic branching and synaptogenesis in cortex and hippocampus. It is not known if exercise results in similar changes.
Exercise enhances dentate gyrus long-term potentiation. Enrichment increases excitatory postsynaptic potential slopes in the dentate gyrus.
Both exercise and enrichment enhance production of certain growth factors and neurotransmitters in the hippocampus.
Two areas of neurobiological research that may benefit from use of the environmental enrichment and exercise models are mouse genetics and studies of recovery of function following brain and spinal injury or disease. For example, enrichment has been shown to enhance function in mice that have been engineered to overexpress Huntington's disease gene products. In addition, enrichment as well as exercise seem to be beneficial for conditions such as stroke and epilepsy.
Neuronal plasticity is a central theme of modern neurobiology, from cellular and molecular mechanisms of synapse formation in Drosophila to behavioural recovery from strokes in elderly humans. Although the methods used to measure plastic responses differ, the stimuli required to elicit plasticity are thought to be activity-dependent. In this article, we focus on the neuronal changes that occur in response to complex stimulation by an enriched environment. We emphasize the behavioural and neurobiological consequences of specific elements of enrichment, especially exercise and learning
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Rosenzweig, M. R. in Development and Evolution of Brain Size 263– 293 (Academic Press, 1979).
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.
Hebb, D. O. The Organization of Behaviour (Wiley, New York, 1949 ).
Hebb, D. O. The effects of early experience on problem-solving at maturity. Am. Psychol. 2, 306–307 (1947).
Wiesel, T. N. & Hubel, D. N. Extent of recovery from the effects of visual deprivation in kittens. J. Neurophysiol. 28, 1060–1072 (1965).
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).
Rosenzweig, M. R. Environmental complexity, cerebral change, and behavior. Am. Psychol. 21, 321–332 ( 1966).
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).
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).
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).
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).
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).
Bennett, E. L. in Neural Mechanisms of Learning and Memory (eds Rosenzweig, M. R. & Bennett, E. L) 279–287 (MIT Press, Cambridge, Massachusetts, 1976).
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).
Holloway, R. L. Dendritic branching: some preliminary results of training and complexity in rat visual cortex. Brain Res. 2, 393– 396 (1966).
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).
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 ).
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).
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.
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).
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).
Walsh, R. N. & Cummins, R. A. Changes in hippocampal neuronal nuclei in response to environmental stimulation. Int. J. Neurosci. 9, 209–212 ( 1979).
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.
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.
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).
Bernstein, L. A study of some enriching variables in a free-environment for rats. J. Psychosomatic Res. 17, 85–88, (1973).
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).
Walsh, R. N. & Cummins, R. A. Mechanisms mediating the production of environmentally induced brain changes. Psychol. Bull. 82, 986–1000 (1975).
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.
Ambrogini, P. et al. Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci. Lett. 286, 21–24 (2000).
Gould, E. et al. Learning enhances adult neurogenesis in the hippocampal formation . Nature Neurosci. 2, 260– 265 (1999).
Greenough, W. T., Cohen, N. J. & Juraska, J. M. New neurons in old brains: learning to survive? Nature Neurosci. 2, 203–205 (1999).
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).
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).
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).
Kempermann, G., Kuhn, H. G. & Gage, F. H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206– 3212 (1998).
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).
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).
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).
Altman, J. Are new neurons formed in the brains of adult mammals? Science 135, 1127–1128 ( 1962).
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).
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).
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).
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).
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).
Volkmar, F. R. & Greenough, W. T. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176, 1445–1447 ( 1972).
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).
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).
Beaulieu, C. & Colonnier, M. The effect of richness of the environment on cat visual cortex. J. Comp. Neurol. 266, 478–494 (1987).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Vanderwolf, C. H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407– 418 (1969).
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).
Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 , 31–39 (1993).
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).
Wang, S., Scott, B. W. & Wojtowicz, J. M. Heterogenous properties of dentate granule neurons in adult rat. J. Neurobiol. 42, 248– 257 (2000).
Calof, A. L. Intrinsic and extrinsic factors regulating vertebrate neurogenesis. Curr. Opin. Neurobiol. 5, 19–27 (1995).
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).
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).
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).
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).
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).
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).
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).
Young, D. et al. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nature Med. 5, 448–453 (1999).
Carro, E. et al. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 20, 2926–2933 (2000).
Gomez-Pinilla, F., Dao, L. & Vannarith, S. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res. 764, 1– 8 (1997).
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).
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.
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).
Kang, H. & Schuman, E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658–1662 ( 1995).
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).
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).
Por, S. B., Bennett, E. L. & Bondy, S. C. Environmental enrichment and neurotransmitter receptors . Behav. Neural Biol. 34, 132– 140 (1982).
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).
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).
Zolman, J. & Morimoto, H. Cerebral changes related to duration of environmental complexity and locomotor activity. J. Comp. Physiol. Psychol. 60, 382–387 ( 1965).
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).
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).
Soares, J. et al. Brain noradrenergic responses to footshock after chronic activity-wheel running. Behav. Neurosci. 113, 558– 566 (1999).
Chaouloff, F. Physical exercise and brain monoamines: a review. Acta Physiol. Scand. 137, 1–13 ( 1989).
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).
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).
Madsen T. M. et al. Increased neurogenesis in a model of electroconvulsive therapy . Biol. Psychiatry 47, 1043– 1049 (2000).
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).
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).
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.
Darymple-Alford, J. C. & Benton, D. Preoperative differential housing and dorsal hippocampal lesions in rats. Behav. Neurosci. 98, 23–34 ( 1984).
Gentile, A. M. & Beheshti, Z. Enrichment versus exercise effects on motor impairments following cortical removals in rats . Behav. Neural Biol. 47, 321– 332 (1987).
Johansson, B. B. Functional outcome in rats transferred to an enriched environment 15 days after focal brain ischemia. Stroke 27, 324 –326 (1996).
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).
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).
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).
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).
Gerlai, R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 19, 177– 181 (1996).
Bennet, E. L. et al. Effects of successive environments on brain measures. Physiol. Behav. 12, 621–631 (1974).
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).
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).
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).
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).
Horner, P. J. & Gage, F. H. Regenerating the damaged nervous system. Nature 407, 963– 970 (2000).
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.
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).
Levine, S. Infantile experience and resistance to physiological stress. Science 126, 405–406 ( 1957).
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).
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).
Francis, D. D. & Meaney, M. J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 9, 128–134 ( 1999).
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).
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).
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).
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).
Hofer, M. A. On the nature and consequences of early loss. Psychosomatic Med. 58, 570–581 ( 1996).
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).
Kolb, B. & Gibb, R. Environmental enrichment and cortical injury: behavioral and anatomical consequences of frontal cortex lesions. Cereb. Cortex 1, 189–198 (1991).
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).
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).
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).
Winocur, G. Environmental influences on cognitive decline in aged rats. Neurobiol. Aging 19, 589–597 ( 1998).
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).
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).
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).
Warren, J. M., Zerweck, C. & Anthony, A. Effects of environmental enrichment on old mice. Dev. Psychobiol. 15, 13–18 (1982).
We thank the reviewers for their helpful comments on our paper. We appreciate the editorial assistance of M. L. Gage and the assistance of L. Kitabayashi in preparation of the figures. We are grateful for the continued support of the Christopher Reeve Paralysis Foundation, The Lookout Fund, The Parkinson's Disease Foundation and the National Institutes of Health.
- SHOLL RING ANALYSIS
A clear overlay with concentric rings at 20 μm intervals is centred over the cell body and the number of times the dendrites intersect the rings are counted.
- THETA RHYTHM
Neural activity with a frequency of 4–8 Hz.
- HEBB–WILLIAMS MAZE
A rectangular field with a start box and a goal box placed at opposite ends of the apparatus. Different configurations are obtained by placing barriers at different points of the field.
About this article
Cite this article
van Praag, H., Kempermann, G. & Gage, F. Neural consequences of enviromental enrichment. Nat Rev Neurosci 1, 191–198 (2000). https://doi.org/10.1038/35044558
Learning to play golf for elderly people with subjective memory complaints: feasibility of a single‐blinded randomized pilot trial
BMC Neurology (2021)
Nature Communications (2021)
Scientific Reports (2021)
Scientific Reports (2021)
Brains in space: the importance of understanding the impact of long-duration spaceflight on spatial cognition and its neural circuitry
Cognitive Processing (2021)