‘Enriched environments’ are a key experimental paradigm to decipher how interactions between genes and environment change the structure and function of the brain across the lifespan of an animal. The regulation of adult hippocampal neurogenesis by environmental enrichment is a prime example of this complex interaction. As each animal in an enriched environment will have a slightly different set of experiences that results in downstream differences between individuals, enrichment can be considered not only as an external source of rich stimuli but also to provide the room for individual behaviour that shapes individual patterns of brain plasticity and thus function.
Subscribe to Journal
Get full journal access for 1 year
only $22.08 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
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).
Xie, H. et al. Enrichment-induced exercise to quantify the effect of different housing conditions: a tool to standardize enriched environment protocols. Behav. Brain Res. 249, 81–89 (2013).
Fares, R. P. et al. Standardized environmental enrichment supports enhanced brain plasticity in healthy rats and prevents cognitive impairment in epileptic rats. PLOS ONE 8, e53888 (2013).
Mohammed, A. H. et al. Environmental enrichment and the brain. Prog. Brain Res. 138, 109–133 (2002).
Van Praag, H., Kempermann, G. & Gage, F. H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1, 191–198 (2000).
Bennett, E. L., Diamond, M. C., Krech, D. & Rosenzweig, M. R. Chemical and anatomical plasticity of brain. Science 146, 610–619 (1964).
Diamond, M. C. Enriching Heredity (The Free Press, 1988). This important book summarizes the state of the enrichment field from the perspective of one of its key players.
Sale, A., Berardi, N. & Maffei, L. Enrich the environment to empower the brain. Trends Neurosci. 32, 233–239 (2009).
Mora, F. Successful brain aging: plasticity, environmental enrichment, and lifestyle. Dialogues Clin. Neurosci. 15, 45–52 (2013).
Redolat, R. & Mesa-Gresa, P. Potential benefits and limitations of enriched environments and cognitive activity on age-related behavioural decline. Curr. Top. Behav. Neurosci. 10, 293–316 (2012).
Kempermann, G., Kuhn, H. G. & Gage, F. H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493–495 (1997). This article presents the first report to show that environmental enrichment has effects at the level of neuronal numbers.
Freund, J. et al. Emergence of Individuality in Genetically Identical Mice. Science 340, 756–759 (2013). This study reveals that longitudinal behavioural trajectories of locomotor activity correlate with interindividual differences in adult neurogenesis.
Brown, R. E. & Milner, P. M. The legacy of Donald O. Hebb: more than the Hebb synapse. Nat. Rev. Neurosci. 4, 1013–1019 (2003).
Rampon, C. et al. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3, 238–244 (2000).
Garthe, A., Roeder, I. & Kempermann, G. Mice in an enriched environment learn more flexibly because of adult hippocampal neurogenesis. Hippocampus 26, 261–271 (2016).
Melani, R., Chelini, G., Cenni, M. C. & Berardi, N. Enriched environment effects on remote object recognition memory. Neuroscience 352, 296–305 (2017).
Duffy, S. N., Craddock, K. J., Abel, T. & Nguyen, P. V. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn. Mem. 8, 26–34 (2001).
Love, J. M., Chazan-Cohen, R., Raikes, H. & Brooks-Gunn, J. What makes a difference: Early Head Start evaluation findings in a developmental context. Monogr. Soc. Res. Child Dev. 78, vii–viii (2013).
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., Krech, D. & Rosenzweig, M. R. The effects of an enriched environment on the histology of the rat cerebral cortex. J. Comp. Neurol. 123, 111–120 (1964).
Rosenzweig, M. R., Krech, D., Bennett, E. L. & Diamond, M. C. Effects of environmental complexity and training on brain chemistry and anatomy: a replication and extension. J. Comp. Physiol. Psychol. 55, 429–437 (1962).
Rampon, C. et al. Effects of environmental enrichment on gene expression in the brain. Proc. Natl Acad. Sci. USA 97, 12880–12884 (2000). This paper presents one of the first studies attempting to relate changes in gene expression to the effects of environmental enrichment on the brain.
Zhang, T.-Y. et al. Environmental enrichment increases transcriptional and epigenetic differentiation between mouse dorsal and ventral dentate gyrus. Nat. Commun. 9, 298 (2018).
Rattazzi, L. et al. Impact of enriched environment on murine T cell differentiation and gene expression profile. Front. Immunol. 7, 381 (2016).
Zhang, Y. et al. Convergent transcriptomics and proteomics of environmental enrichment and cocaine identifies novel therapeutic strategies for addiction. Neuroscience 339, 254–266 (2016).
Ragu Varman, D. & Rajan, K. E. Environmental enrichment reduces anxiety by differentially activating serotonergic and neuropeptide Y (NPY)-ergic system in Indian field mouse (Mus booduga): an animal model of post-traumatic stress disorder. PLOS ONE 10, e0127945 (2015).
Gualtieri, F. et al. Effects of environmental enrichment on doublecortin and BDNF expression along the dorso-ventral axis of the dentate gyrus. Front. Neurosci. 11, 189–115 (2017).
Sztainberg, Y., Kuperman, Y., Tsoory, M., Lebow, M. & Chen, A. The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1. Mol. Psychiatry 15, 905–917 (2010).
Singhal, G., Jaehne, E. J., Corrigan, F. & Baune, B. T. Cellular and molecular mechanisms of immunomodulation in the brain through environmental enrichment. Front. Cell. Neurosci. 8, 97 (2014).
Vega-Rivera, N. M. et al. The neurogenic effects of an enriched environment and its protection against the behavioral consequences of chronic mild stress persistent after enrichment cessation in six-month-old female Balb/C mice. Behav. Brain Res. 301, 72–83 (2016).
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).
Nithianantharajah, J. & Hannan, A. J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 7, 697–709 (2006). This important review article provides a large overview of disease-related effects of environmental enrichment.
Kempermann, G., Gast, D. & Gage, F. H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 52, 135–143 (2002).
Diamond, M. C., Johnson, R. E., Protti, A. M. & Ott, C. Plasticity in the 904-day-old male rat cerebral cortex. Exp. Neurol. 87, 309–317 (1985). This historically important study extends enrichment research to very old animals.
Maruoka, T., Kodomari, I., Yamauchi, R., Wada, E. & Wada, K. Maternal enrichment affects prenatal hippocampal proliferation and open-field behaviors in female offspring mice. Neurosci. Lett. 454, 28–32 (2009).
Arai, J. A., Li, S., Hartley, D. M. & Feig, L. A. Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment. J. Neurosci. 29, 1496–1502 (2009).
Bechard, A. R. & Lewis, M. H. Transgenerational effects of environmental enrichment on repetitive motor behavior development. Behav. Brain Res. 307, 145–149 (2016).
Yeshurun, S., Short, A. K., Bredy, T. W., Pang, T. Y. & Hannan, A. J. Paternal environmental enrichment transgenerationally alters affective behavioral and neuroendocrine phenotypes. Psychoneuroendocrinology 77, 225–235 (2017).
Arai, J. A. & Feig, L. A. Long-lasting and transgenerational effects of an environmental enrichment on memory formation. Brain Res. Bull. 85, 30–35 (2011).
Smits, B. M. G., van Zutphen, B. F. M., Plasterk, R. H. A. & Cuppen, E. Genetic variation in coding regions between and within commonly used inbred rat strains. Genome Res. 14, 1285–1290 (2004).
Sauce, B. et al. The impact of environmental interventions among mouse siblings on the heritability and malleability of general cognitive ability. Phil. Trans. R. Soc. B 373, 20170289 (2018).
Kobilo, T. et al. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn. Mem. 18, 605–609 (2011).
Walsh, R. N. & Cummins, R. A. Mechanisms mediating the production of environmentally induced brain changes. Psychol. Bull. 82, 986–1000 (1975). This important conceptual article develops influential ideas of how enrichment acts on the brain.
Welch, B. L., Brown, D. G., Welch, A. S. & Lin, D. C. Isolation, restrictive confinement or crowding of rats for one year. I. Weight, nucleic acids and protein of brain regions. Brain Res. 75, 71–84 (1974).
Cummins, R. A., Livesey, P. J. & Evans, J. G. A developmental theory of environmental enrichment. Science 197, 692–694 (1977). Complementary to reference 43, this article further refines the mechanistic ideas about environmental enrichment as prevalent during the high days of the field in the mid-1970s.
Van Praag, H., Kempermann, G. & Gage, F. H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266–270 (1999).
Eisinger, B. E. & Zhao, X. Identifying molecular mediators of environmentally enhanced neurogenesis. Cell Tissue Res. 371, 7–21 (2017).
Craver, C. F. & Darden, L. In Search of Mechanisms: Discoveries Across the Life Sciences (Univ. of Chicago Press, 2013). This article provides a very good discussion of the challenges and limitations of mechanistic insight in biology.
Bekinschtein, P., Oomen, C. A., Saksida, L. M. & Bussey, T. J. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin. Cell Dev. Biol. 22, 536–542 (2011).
Tyagi, E., Zhuang, Y., Agrawal, R., Ying, Z. & Gomez-Pinilla, F. Interactive actions of Bdnf methylation and cell metabolism for building neural resilience under the influence of diet. Neurobiol. Dis. 73, 307–318 (2015).
Kempermann, G. Cynefin as reference framework to facilitate insight and decision-making in complex contexts of biomedical research. Front. Neurosci. 11, 634 (2017).
Yazdani, A. & Boerwinkle, E. Causal inference in the age of decision medicine. J. Data Mining Genomics Proteomics 6, 1–6 (2015).
Jones, D. G. & Smith, B. J. The hippocampus and its response to differential environments. Prog. Neurobiol. 15, 19–69 (1980).
Ohline, S. M. & Abraham, W. C. Environmental enrichment effects on synaptic and cellular physiology of hippocampal neurons. Neuropharmacology. https://doi.org/10.1016/j.neuropharm.2018.04.007 (2018).
Bilkey, D. K. et al. Exposure to complex environments results in more sparse representations of space in the hippocampus. Hippocampus 27, 1178–1191 (2017).
Fischer, A. Environmental enrichment as a method to improve cognitive function. What can we learn from animal models? Neuroimage 131, 42–47 (2016).
Tanti, A. et al. Region-dependent and stage-specific effects of stress, environmental enrichment, and antidepressant treatment on hippocampal neurogenesis. Hippocampus 23, 797–811 (2013).
Zheng, J. et al. Adult hippocampal neurogenesis along the dorsoventral axis contributes differentially to environmental enrichment combined with voluntary exercise in alleviating chronic inflammatory pain in mice. J. Neurosci. 37, 4145–4157 (2017).
Kempermann, G. The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci. 31, 163–169 (2008). This paper presents an early discussion of the relevance of adult hippocampal neurogenesis from a lifespan perspective, building upon the findings that environmental enrichment stimulates adult neurogenesis.
Schloesser, R. J., Lehmann, M., Martinowich, K., Manji, H. K. & Herkenham, M. Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol. Psychiatry 15, 1152–1163 (2010).
Sorrells, S. F. et al. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555, 377–381 (2018).
Boldrini, M. et al. Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell 22, 589–599 (2018).
Knoth, R. et al. Murine features of neurogenesis in the human Hippocampus across the lifespan from 0 to 100 years. PLOS ONE 5, e8809 (2010).
Eriksson, P. S. et al. Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313–1317 (1998).
Ernst, A. et al. Neurogenesis in the striatum of the adult human brain. Cell 156, 1072–1083 (2014).
Spalding, K. L. et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 153, 1227 (2013). This key publication (after the historical reference 64) confirms adult neurogenesis in the human hippocampus with novel methods and provides a quantitative model.
Kempermann, G. et al. Human adult neurogenesis: evidence and remaining questions. Cell Stem Cell 23, 25–30 (2018).
Kronenberg, G. et al. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467, 455–463 (2003).
Zhao, C., Jou, J., Wolff, L. J., Sun, H. & Gage, F. H. Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers. J. Comp. Neurol. 522, 2756–2766 (2014).
Tashiro, A., Makino, H. & Gage, F. H. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci. 27, 3252–3259 (2007).
Anstötz, M., Lee, S. K., Neblett, T. I., Rune, G. M. & Maccaferri, G. Experience-dependent regulation of Cajal–Retzius cell networks in the developing and adult mouse hippocampus. Cereb. Cortex 28, 672–687 (2017).
Kempermann, G., Brandon, E. P. & Gage, F. H. Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr. Biol. 8, 939–942 (1998).
Brandt, M. D., Jessberger, S. & Steiner, B. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol. Cell. Neurosci. 24, 603–613 (2003).
Garthe, A., Behr, J. & Kempermann, G. Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLOS ONE 4, e5464 (2009).
Schmidt-Hieber, C., Jonas, P. & Bischofberger, J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184–187 (2004).
Wang, J. W., David, D. J., Monckton, J. E., Battaglia, F. & Hen, R. Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 28, 1374–1384 (2008).
Saxe, M. D. et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl Acad. Sci. USA 103, 17501–17506 (2006).
Marín-Burgin, A., Mongiat, L. A., Pardi, M. B. & Schinder, A. F. Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335, 1238–1242 (2012).
Kirschen, G. W. et al. Active dentate granule cells encode experience to promote the addition of adult-born hippocampal neurons. J. Neurosci. 37, 4661–4678 (2017).
Döbrössy, M. D. et al. Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol. Psychiatry 8, 974–982 (2003).
Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T. J. Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260–265 (1999). This early study shows that learning can induce adult neurogenesis, supporting the idea that learning is also a relevant stimulus for enrichment effects on adult neurogenesis.
Leuner, B. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J. Neurosci. 24, 7477–7481 (2004).
Hairston, I. S. et al. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J. Neurophysiol. 94, 4224–4233 (2005).
Fabel, K. et al. Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front. Neurosci. 3, 50 (2009).
Iggena, D. et al. Only watching others making their experiences is insufficient to enhance adult neurogenesis and water maze performance in mice. Sci. Rep. 5, 14141 (2015).
Kempermann, G., Kuhn, H. G. & Gage, F. H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18, 3206–3212 (1998).
Kronenberg, G. et al. Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol. Aging 27, 1505–1513 (2006).
Levone, B. R., Cryan, J. F. & O’Leary, O. F. Role of adult hippocampal neurogenesis in stress resilience. Neurobiol. Stress 1, 147–155 (2015).
Anacker, C. et al. Hippocampal neurogenesis confers stress resilience by inhibiting the ventral dentate gyrus. Nature 559, 98–102 (2018). This key study highlights how adult-born neurons in the ventral hippocampus might contribute to key functions in affective behaviour and to coping with stress.
Keyvani, K., Sachser, N., Witte, O. W. & Paulus, W. Gene expression profiling in the intact and injured brain following environmental enrichment. J. Neuropathol. Exp. Neurol. 63, 598–609 (2004).
Lacar, B. et al. Nuclear RNA-seq of single neurons reveals molecular signatures of activation. Nat. Commun. 7, 11022 (2016).
Steiner, B., Zurborg, S., Hörster, H., Fabel, K. & Kempermann, G. Differential 24 h responsiveness of Prox1-expressing precursor cells in adult hippocampal neurogenesis to physical activity, environmental enrichment, and kainic acid-induced seizures. Neuroscience 154, 521–529 (2008).
Kempermann, G. Seven principles in the regulation of adult neurogenesis. Eur. J. Neurosci. 33, 1018–1024 (2011).
Snyder, J. S., Kee, N. & Wojtowicz, J. M. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85, 2423–2431 (2001).
Clelland, C. D. et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210–213 (2009).
Sahay, A. et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466–470 (2011).
Walsh, R. N. & Cummins, R. A. Changes in hippocampal neuronal nuclei in response to environmental stimulation. Int. J. Neurosci. 9, 209–212 (1979).
Wolfer, D. P. et al. Laboratory animal welfare: cage enrichment and mouse behaviour. Nature 432, 821–822 (2004). This much discussed report brings up the question of whether environmental enrichment might affect the reproducibility of laboratory experiments by increasing variability.
André, V. et al. Laboratory mouse housing conditions can be improved using common environmental enrichment without compromising data. PLOS Biol. 16, e2005019 (2018).
Richter, S. H., Garner, J. P. & Würbel, H. Environmental standardization: cure or cause of poor reproducibility in animal experiments? Nat. Methods 6, 257–261 (2009).
Freund, J. et al. Association between exploratory activity and social individuality in genetically identical mice living in the same enriched environment. Neuroscience 309, 140–152 (2015).
Torquet, N. et al. Social interactions impact on the dopaminergic system and drive individuality. Nat. Commun. 9, 3081 (2018).
Loseva, E., Yuan, T.-F. & Karnup, S. Genetics and human agency: comment on Dar-Nimrod and Heine (2011). Psychol. Bull. 137, 825–828 (2011).
Cotel, M. C., Jawhar, S., Christensen, D. Z., Bayer, T. A. & Wirths, O. Environmental enrichment fails to rescue working memory deficits, neuron loss, and neurogenesis in APP/PS1KI mice. NBA 33, 96–107 (2012).
Salmin, V. V. et al. Differential roles of environmental enrichment in Alzheimer’s type of neurodegeneration and physiological aging. Front. Aging Neurosci. 9, 435–412 (2017).
Hollands, C., Bartolotti, N. & Lazarov, O. Alzheimer’s disease and hippocampal adult neurogenesis; exploring shared mechanisms. Front. Neurosci. 10, 178 (2016).
Norton, S., Matthews, F. E., Barnes, D. E., Yaffe, K. & Brayne, C. Potential for primary prevention of Alzheimer’s disease: an analysis of population-based data. Lancet Neurol. 13, 788–794 (2014). This very important analysis underscores the role of lifestyle interventions in the prevention of AD, but in principle is extendable to other disease conditions.
Hüttenrauch, M., Walter, S., Kaufmann, M., Weggen, S. & Wirths, O. Limited effects of prolonged environmental enrichment on the pathology of 5XFAD mice. Mol. Neurobiol. 54, 6542–6555 (2017).
Habeck, C. et al. Cognitive reserve and brain maintenance: orthogonal concepts in theory and practice. Cereb. Cortex 27, 3962–3969 (2016).
Scarmeas, N. & Stern, Y. Cognitive reserve and lifestyle. J. Clin. Exp. Neuropsychol. 25, 625–633 (2003).
Gelfo, F., Mandolesi, L., Serra, L., Sorrentino, G. & Caltagirone, C. The neuroprotective effects of experience on cognitive functions: evidence from animal studies on the neurobiological bases of brain reserve. Neuroscience 370, 218–235 (2018).
Petrosini, L. et al. On whether the environmental enrichment may provide cognitive and brain reserves. Brain Res. Rev. 61, 221–239 (2009).
Hertzog, C., Kramer, A. F., Wilson, R. S. & Lindenberger, U. Enrichment effects on adult cognitive development: can the functional capacity of older adults be preserved and enhanced? Psychol. Sci. Public Interest 9, 1–65 (2008). This extremely comprehensive and insightful review captures the state of ‘enrichment’ concepts under the human condition.
Johansson, B. B. Brain plasticity and stroke rehabilitation. The Willis lecture. Stroke 31, 223–230 (2000).
Janssen, H. et al. An enriched environment improves sensorimotor function post-ischemic stroke. Neurorehabil. Neural Repair 24, 802–813 (2010).
Hermann, D. M. & Chopp, M. Promoting neurological recovery in the post-acute stroke phase: benefits and challenges. Eur. Neurol. 72, 317–325 (2014).
Morgan, C., Novak, I. & Badawi, N. Enriched environments and motor outcomes in cerebral palsy: systematic review and meta-analysis. Pediatrics 132, e735–e746 (2013).
Corbett, D., Jeffers, M., Nguemeni, C., Gomez-Smith, M. & Livingston-Thomas, J. Lost in translation: rethinking approaches to stroke recovery. Prog. Brain Res. 218, 413–434 (2015).
Scarr, S. & McCartney, K. How people make their own environments: a theory of genotype greater than environment effects. Child Dev. 54, 424–435 (1983). This classical paper discusses the effects of genotype on shaping and refining living environments.
Beans, C. What happens when lab animals go wild. Proc. Natl Acad. Sci. USA 115, 3196–3199 (2018).
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).
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).
Chalfin, L. et al. Mapping ecologically relevant social behaviours by gene knockout in wild mice. Nat. Commun. 5, 4569 (2014).
Abolins, S. et al. The comparative immunology of wild and laboratory mice. Mus musculus domesticus. Nat. Commun. 8, 14811 (2017).
Smith, J., Hurst, J. L. & Barnard, C. J. Comparing behaviour in wild and laboratory strains of the house mouse: levels of comparison and functional inference. Behav. Processes 32, 79–86 (1994).
David, J. M., Knowles, S., Lamkin, D. M. & Stout, D. B. Individually ventilated cages impose cold stress on laboratory mice: a source of systemic experimental variability. J. Am. Assoc. Lab. Anim. Sci. 52, 738–744 (2013).
The author thanks the members of his group who in many discussions contributed to shaping the ideas presented in this article.
Nature Reviews Neuroscience thanks A. Hannan and the other anonymous reviewers for their contribution to the peer review of this work.
The author declares no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
- Adjuvant manipulation
A supportive treatment that is applied alongside a primary (therapeutic) intervention.
A school of thought in cognitive psychology that treated higher brain functions and especially learning as consequence of more or less simple input–output relationships (‘psychic reflexes’).
- Emergent properties
Properties that arise in complex systems and go beyond what can be predicted from knowing the functions of the parts of that system.
- Enriched environments
(ENRs). Defined housing conditions for laboratory animals that are richer in stimuli than standard conditions.
The processes by which members of a population become different from each other.
- Outbred strains
Laboratory strains of animals that preserve a certain level of genetic inhomogeneity (as opposed to inbred strains, in which animals are genetically identical).
About this article
Cite this article
Kempermann, G. Environmental enrichment, new neurons and the neurobiology of individuality. Nat Rev Neurosci 20, 235–245 (2019). https://doi.org/10.1038/s41583-019-0120-x
Behavioural Brain Research (2020)
Frontiers in Neuroscience (2020)
Energy Restriction Enhances Adult Hippocampal Neurogenesis-Associated Memory after Four Weeks in an Adult Human Population with Central Obesity; a Randomized Controlled Trial
Cellular and Molecular Neurobiology (2020)
Frontiers in Aging Neuroscience (2020)