Cellular and molecular mechanisms of immunomodulation in the brain through environmental enrichment
Open accessAbstract
Recent studies on environmental enrichment (EE) have shown cytokines, cellular immune components [e.g., T lymphocytes, natural killer (NK) cells], and glial cells in causal relationship to EE in bringing out changes to neurobiology and behavior. The purpose of this review is to evaluate these neuroimmune mechanisms associated with neurobiological and behavioral changes in response to different EE methods. We systematically reviewed common research databases. After applying all inclusion and exclusion criteria, 328 articles remained for this review. Physical exercise (PE), a form of EE, elicits anti-inflammatory and neuromodulatory effects through interaction with several immune pathways including interleukin (IL)-6 secretion from muscle fibers, reduced expression of Toll-like receptors on monocytes and macrophages, reduced secretion of adipokines, modulation of hippocampal T cells, priming of microglia, and upregulation of mitogen-activated protein kinase phosphatase-1 in central nervous system. In contrast, immunomodulatory roles of other enrichment methods are not studied extensively. Nonetheless, studies showing reduction in the expression of IL-1β and tumor necrosis factor-α in response to enrichment with novel objects and accessories suggest anti-inflammatory effects of novel environment. Likewise, social enrichment, though considered a necessity for healthy behavior, results in immunosuppression in socially defeated animals. This has been attributed to reduction in T lymphocytes, NK cells and IL-10 in subordinate animals. EE through sensory stimuli has been investigated to a lesser extent and the effect on immune factors has not been evaluated yet. Discovery of this multidimensional relationship between immune system, brain functioning, and EE has paved a way toward formulating environ-immuno therapies for treating psychiatric illnesses with minimal use of pharmacotherapy. While the immunomodulatory role of PE has been evaluated extensively, more research is required to investigate neuroimmune changes associated with other enrichment methods.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The inflammasome plays a role in depressive- and anxiety-like behaviors and locomotor activity.
“Among those pathways, researchers showed that the inflammasome plays a role in depressive- and anxiety-like behaviors, and locomotor activity (57).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [57]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & the PRISMA Group* (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-151-4-200908180-00135 · Cited by 37,554 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000100 · Cited by 28,164 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2009.06.005 · Cited by 19,575 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-151-4-200908180-00136 · Cited by 10,349 · see citing works
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023 · see citing works
Glutamate neurotoxicity and diseases of the nervous system
Choi, D. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90162-6 · Cited by 8,152 · see citing works
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
Exercise training increases size of hippocampus and improves memory
Erickson, K. I., Voss, M. W., Prakash, R. S., Basak, C., Szabo, A., Chaddock, L., Kim, J. S., Heo, S., Alves, H., White, S. M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015950108 · Cited by 4,855 · see citing works
Microglia: a sensor for pathological events in the CNS
Kreutzberg, G. W. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)10049-7 · Cited by 4,396 · see citing works
Toll-like receptors and innate immunity
Medzhitov, R. (2001) · Nature Reviews Immunology · doi:10.1038/35100529 · Cited by 4,308 · see citing works
Toll-like receptor control of the adaptive immune responses
Iwasaki, A., & Medzhitov, R. M. (2004) · Nature Immunology · doi:10.1038/ni1112 · Cited by 4,166 · see citing works
Be smart, exercise your heart: Exercise effects on brain and cognition
Hillman, C. H., Erickson, K. I., & Kramer, A. F. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2298 · Cited by 3,563 · see citing works
A protein kinase involved in the regulation of inflammatory cytokine biosynthesis
Lee, J. C., Laydon, J. T., McDonnell, P., Gallagher, T. F., Kumar, S., Green, D., McNulty, D. E., Blumenthal, M. J., Keys, J., vatter, S. W. L., et al. (1994) · Nature · doi:10.1038/372739a0 · Cited by 3,266 · see citing works
The anti-inflammatory effect of exercise
Petersen, A. M. W., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00164.2004 · Cited by 3,100 · cited 1× · see citing works
“It is clear that PE affects skeletal muscles which are able to act as an endocrine organ in body as they release myokines/cytokines on contraction thereby influencing metabolism and modifying cytokine production in other tissues and organs (Petersen and Pedersen, 2006).”
BackgroundSocioeconomic inequalities in depression: a meta-analysis
Lorant, V. (2003) · American Journal of Epidemiology · doi:10.1093/aje/kwf182 · Cited by 2,603 · see citing works
Gleeson, M., Bishop, N. C., Stensel, D. J., Lindley, M. R., Mastana, S. S., & Nimmo, M. A. (2011) · Nature Reviews Immunology · doi:10.1038/nri3041 · Cited by 2,470 · see citing works
Gender differences in depression: Critical review
Piccinelli, M., & Wilkinson, G. (2000) · British Journal of Psychiatry · doi:10.1192/bjp.177.6.486 · Cited by 2,376 · cited 2× · see citing works
“REVIEW ARTICLE published: 03 April 2014 doi: 10.3389/fncel.2014.00097 Cellular and molecular mechanisms of immunomodulation in the brain through environmental enrichment”
InfluentialChanges in grey matter induced by training
Draganski, B., Gaser, C., Busch, V., Schuierer, G., Bogdahn, U., & May, A. (2004) · Nature · doi:10.1038/427311a · Cited by 2,373 · see citing works
Exercise builds brain health: key roles of growth factor cascades and inflammation
Cotman, C. W., Berchtold, N. C., & Christie, L.-A. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.06.011 · Cited by 2,268 · see citing works
Insights into the ageing mind: a view from cognitive neuroscience
Hedden, T., & Gabrieli, J. D. E. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1323 · Cited by 2,223 · see citing works
An active and socially integrated lifestyle in late life might protect against dementia
Fratiglioni, L., Paillard-Borg, S., & Winblad, B. (2004) · The Lancet Neurology · doi:10.1016/s1474-4422(04)00767-7 · Cited by 2,135 · see citing works
Aerobic Exercise Training Increases Brain Volume in Aging Humans
Colcombe, S. J., Erickson, K. I., Scalf, P. E., Kim, J. S., Prakash, R., McAuley, E., Elavsky, S., Marquez, D. X., Hu, L., & Kramer, A. F. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.11.1166 · Cited by 2,134 · see citing works
Exercise enhances learning and hippocampal neurogenesis in aged mice
van Praag, H., Shubert, T., Zhao, C., & Gage, F. H. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-05.2005 · Cited by 2,078 · see citing works
Opal, S. M., & DePalo, V. A. (2000) · Chest · doi:10.1378/chest.117.4.1162 · Cited by 1,752 · see citing works
Exercise and the immune system: regulation, integration, and adaptation
Pedersen, B. K., & Hoffman-Goetz, L. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.3.1055 · Cited by 1,710 · see citing works
A Meta-Analysis of Cognitive Remediation for Schizophrenia: Methodology and Effect Sizes
Wykes, T., Huddy, V., Cellard, C., McGurk, S. R., & Czobor, P. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2010.10060855 · Cited by 1,693 · see citing works
MAP Kinases in the Immune Response
Dong, C., Davis, R. J., & Flavell, R. A. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.091301.131133 · Cited by 1,660 · see citing works
Cognitive neuroscience of human social behaviour
Adolphs, R. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1056 · Cited by 1,657 · see citing works
Microglia as a source and target of cytokines
Hanisch, U. (2002) · Glia · doi:10.1002/glia.10161 · Cited by 1,645 · cited 2× · see citing works
“…their overexpression or sustained stimulation can result in enhanced production of cytokines (e.g., IL-1β and TNF-α; Sawada et al., 1989; Hanisch, 2002), as well as in the expression of class I and II major histocompatibility complex antigens as seen in a RCT in rodents and in the…”
BackgroundLong-term Effects of Cognitive Training on Everyday Functional Outcomes in Older Adults
Willis, S. L., Tennstedt, S. L., Marsiske, M., Ball, K., Elias, J., Koepke, K. M., Morris, J. N., Rebok, G. W., Unverzagt, F. W., Stoddard, A. M., et al. (2006) · JAMA · doi:10.1001/jama.296.23.2805 · Cited by 1,496 · see citing works
Immune modulation of learning, memory, neural plasticity and neurogenesis
Yirmiya, R., & Goshen, I. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.015 · Cited by 1,483 · see citing works
Association between obesity and psychiatric disorders in the US adult population
Simon, G. E., Von Korff, M., Saunders, K., Miglioretti, D. L., Crane, P. K., van Belle, G., & Kessler, R. C. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.7.824 · Cited by 1,338 · see citing works
Gene–environment interactions in psychiatry: joining forces with neuroscience
Caspi, A., & Moffitt, T. E. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1925 · Cited by 1,300 · see citing works
Dong, Y., & Benveniste, E. N. (2001) · Glia · doi:10.1002/glia.1107 · Cited by 1,296 · see citing works
MCGEER, P., & MCGEER, E. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(95)00011-9 · Cited by 1,287 · see citing works
Activation of the primary visual cortex by Braille reading in blind subjects
Sadato, N., Pascual-Leone, A., Grafman, J., Ibañez, V., Deiber, M.-P., Dold, G., & Hallett, M. (1996) · Nature · doi:10.1038/380526a0 · Cited by 1,253 · see citing works
A Meta-Analysis of Cognitive Remediation in Schizophrenia
McGurk, S. R., Twamley, E. W., Sitzer, D. I., McHugo, G. J., & Mueser, K. T. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07060906 · Cited by 1,214 · see citing works
Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J., & Schwartz, M. (2006) · Nature Neuroscience · doi:10.1038/nn1629 · Cited by 1,209 · see citing works
Immune system to brain signaling: Neuropsychopharmacological implications
Capuron, L., & Miller, A. H. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2011.01.014 · Cited by 1,195 · see citing works
T‐lymphocyte entry into the central nervous system
Hickey, W. F., Hsu, B. L., & Kimura, H. (1991) · Journal of Neuroscience Research · doi:10.1002/jnr.490280213 · Cited by 1,176 · see citing works
Maier, S. F., & Watkins, L. R. (1998) · Psychological Review · doi:10.1037/0033-295x.105.1.83 · Cited by 1,130 · see citing works
Blood, A. J., Zatorre, R. J., Bermudez, P., & Evans, A. C. (1999) · Nature Neuroscience · doi:10.1038/7299 · Cited by 1,097 · see citing works
Liu, B., & Hong, J.-S. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.035048 · Cited by 1,095 · see citing works
Tansey, M. G., & Goldberg, M. S. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.11.004 · Cited by 1,045 · see citing works
Effects of acute bouts of exercise on cognition
Tomporowski, P. D. (2003) · Acta Psychologica · doi:10.1016/s0001-6918(02)00134-8 · Cited by 1,030 · see citing works
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
Broad Expression of Toll-Like Receptors in the Human Central Nervous System
Bsibsi, M., Ravid, R., Gveric, D. O., & van Noort, J. M. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.11.1013 · Cited by 1,000 · see citing works
Beneficial effects of physical exercise on neuroplasticity and cognition
Hötting, K., & Röder, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.005 · Cited by 991 · see citing works
Neurotrophins regulate dendritic growth in developing visual cortex
McAllister, A. K., Lo, D. C., & Katz, L. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90171-x · Cited by 959 · see citing works
Amygdala activity related to enhanced memory for pleasant and aversive stimuli
Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D. (1999) · Nature Neuroscience · doi:10.1038/6404 · Cited by 913 · see citing works
Music listening enhances cognitive recovery and mood after middle cerebral artery stroke
Särkämö, T., Tervaniemi, M. H., Laitinen, S., Forsblom, A., Soinila, S. O., Mikkonen, M., Autti, T. H., Silvennoinen, H. M., Erkkilä, J., Laine, M., et al. (2008) · Brain · doi:10.1093/brain/awn013 · Cited by 905 · see citing works
Kempermann, G., Gast, D., & Gage, F. H. (2002) · Annals of Neurology · doi:10.1002/ana.10262 · Cited by 889 · see citing works
Environmental Enrichment Reduces Aβ Levels and Amyloid Deposition in Transgenic Mice
Lazarov, O., Robinson, J., Tang, Y.-P., Hairston, I. S., Korade-Mirnics, Z., Lee, V. M.-Y., Hersh, L. B., Sapolsky, R. M., Mirnics, K., & Sisodia, S. S. (2005) · Cell · doi:10.1016/j.cell.2005.01.015 · Cited by 885 · see citing works
Efficacy of an evidence-based cognitive stimulation therapy programme for people with dementia
Spector, A. E., Thorgrimsen, L., Woods, B. T., Royan, L., Davies, S., Butterworth, M., & Orrell, M. W. (2003) · The British Journal of Psychiatry · doi:10.1192/bjp.183.3.248 · Cited by 880 · see citing works
Aalbers, S., Fusar-Poli, L., Freeman, R. E., Spreen, M., Ket, J. C., Vink, A. C., Maratos, A., Crawford, M., Chen, X.-J., & Gold, C. (2017) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004517.pub3 · Cited by 838 · see citing works
Contribution of human hippocampal region to novelty detection
Knight, R. T. (1996) · Nature · doi:10.1038/383256a0 · Cited by 834 · see citing works
Zald, D. H., & Pardo, J. V. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.8.4119 · Cited by 826 · see citing works
Function of C-reactive protein
Clos, T. W. D. (2000) · Annals of Medicine · doi:10.3109/07853890009011772 · Cited by 808 · see citing works
Brain inflammation and adult neurogenesis: The dual role of microglia
Ekdahl, C. T., Kokaia, Z., & Lindvall, O. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.052 · Cited by 801 · see citing works
Inflammatory processes in Alzheimer's disease
Heneka, M. T., & O'Banion, M. K. (2007) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.11.017 · Cited by 782 · see citing works
Passage of cytokines across the blood–brain barrier
Banks, W. A., Kastin, A. J., & Broadwell, R. D. (1996) · Neuroimmunomodulation · doi:10.1159/000097202 · Cited by 778 · see citing works
Temporal and spatial dynamics of brain structure changes during extensive learning
Draganski, B., Gaser, C., Kempermann, G., Kuhn, H. G., Winkler, J., Buchel, C., & May, A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4628-05.2006 · Cited by 765 · see citing works
Circulating Insulin-Like Growth Factor I Mediates Effects of Exercise on the Brain
Carro, E., Nuñez, A., Busiguina, S., & Torres-Aleman, I. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02926.2000 · Cited by 762 · see citing works
Evidence for a cytokine model of cognitive function
McAfoose, J., & Baune, B. T. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.10.005 · Cited by 760 · see citing works
Self-citationAnderson, D. H., Radeke, M. J., Gallo, N. B., Chapin, E. A., Johnson, P. T., Curletti, C. R., Hancox, L. S., Hu, J., Ebright, J. N., Malek, G., et al. (2010) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2009.11.003 · Cited by 727 · see citing works
Training-Induced Brain Structure Changes in the Elderly
Boyke, J., Driemeyer, J., Gaser, C., Büchel, C., & May, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0742-08.2008 · Cited by 681 · see citing works
Rochefort, C., Gheusi, G., Vincent, J., & Lledo, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02679.2002 · Cited by 678 · see citing works
Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity
Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07840.2002 · Cited by 663 · see citing works
The olfactory bulbectomized rat as a model of depression: An update
Kelly, J. P., Wrynn, A. S., & Leonard, B. E. (1997) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(97)00004-1 · Cited by 662 · see citing works
Do early‐life events permanently alter behavioral and hormonal responses to stressors?
Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00025-2 · Cited by 654 · see citing works
Early-life programming of later-life brain and behavior: a critical role for the immune system
Bilbo, S. D. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.014.2009 · Cited by 652 · cited 2× · see citing works
“When exposed to perinatal infection and neonatal maternal separation in controlled trials, rodents displayed marked cognitive and behavioral changes, and impaired learning and memory which persisted throughout their lifespan (Bilbo and Schwarz, 2009; Vivinetto et al., 2013).”
BackgroundTowards a neural basis of music-evoked emotions
Koelsch, S. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.01.002 · Cited by 651 · see citing works
Mesholam, R. I., Moberg, P. J., Mahr, R. N., & Doty, R. L. (1998) · Archives of Neurology · doi:10.1001/archneur.55.1.84 · Cited by 643 · see citing works
Production of tumor necrosis factor-alpha by microglia and astrocytes in culture
Sawada, M., Kondo, N., Suzumura, A., & Marunouchi, T. (1989) · Brain Research · doi:10.1016/0006-8993(89)90078-4 · Cited by 631 · see citing works
Inflammation and neurodegeneration in Parkinson's disease
McGeer, P. L., & McGeer, E. G. (2004) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2004.01.005 · Cited by 628 · see citing works
Early life experience alters response of adult neurogenesis to stress
Mirescu, C., Peters, J. D., & Gould, E. (2004) · Nature Neuroscience · doi:10.1038/nn1290 · Cited by 625 · see citing works
Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., Fabbri, M. E., Tessarollo, L., Maffei, L., Berardi, N., et al. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05059.x · Cited by 619 · see citing works
Biernaskie, J. A., & Corbett, D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05272.2001 · Cited by 608 · see citing works
Animal models of social stress: Effects on behavior and brain neurochemical systems
Blanchard, R. J., McKittrick, C. R., & Blanchard, D. C. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00449-8 · Cited by 595 · see citing works
Glia and their cytokines in progression of neurodegeneration
Mrak, R. E., & Griffin, W. S. T. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.05.010 · Cited by 592 · see citing works
Clare, L., & Woods, B. (2003) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003260 · Cited by 576 · see citing works
Long-Term Environmental Enrichment Leads to Regional Increases in Neurotrophin Levels in Rat Brain
Ickes, B. R., Pham, T. M., Sanders, L., Albeck, D. S., Mohammed, A. H. S., & Granholm, A. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7415 · Cited by 541 · see citing works
Prenatal Infection as a Risk Factor for Schizophrenia
Brown, A. S. (2006) · Schizophrenia Bulletin · doi:10.1093/schbul/sbj052 · Cited by 540 · see citing works
Devanand, D. P., Marston, K., Liu, X., Pelton, G. H., Padilla, M., Marder, K. S., Bell, K. L., Stern, Y., & Mayeux, R. P. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.9.1399 · Cited by 536 · see citing works
Iron Deficiency Alters Brain Development and Functioning
Beard, J. (2003) · Journal of Nutrition · doi:10.1093/jn/133.5.1468s · Cited by 534 · see citing works
Anti-Inflammatory Actions of Intravenous Immunoglobulin
Nimmerjahn, F., & Ravetch, J. V. (2008) · Annual Review of Immunology · doi:10.1146/annurev.immunol.26.021607.090232 · Cited by 526 · see citing works
The blood-brain barrier and immune function and dysfunction
Banks, W. A., & Erickson, M. A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.07.031 · Cited by 523 · see citing works
Wu, A., Ying, Z., & Gomez-Pinilla, F. (2004) · Journal of Neurotrauma · doi:10.1089/neu.2004.21.1457 · Cited by 518 · see citing works
Environmental Enrichment Mitigates Cognitive Deficits in a Mouse Model of Alzheimer's Disease
Jankowsky, J. L., Melnikova, T., Fadale, D. J., Xu, G. M., Slunt, H. H., Gonzales, V., Younkin, L. H., Younkin, S. G., Borchelt, D. R., & Savonenko, A. V. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.5080-04.2005 · Cited by 517 · see citing works
Exercise as a Mean to Control Low‐Grade Systemic Inflammation
Mathur, N., & Pedersen, B. K. (2008) · Mediators of Inflammation · doi:10.1155/2008/109502 · Cited by 514 · see citing works
Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex.
Castrén, E., Zafra, F., Thoenen, H., & Lindholm, D. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.20.9444 · Cited by 513 · see citing works
Inhibitory role for GABA in autoimmune inflammation
Bhat, R., Axtell, R., Mitra, A., Miranda, M., Lock, C., Tsien, R. W., & Steinman, L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0915139107 · Cited by 509 · see citing works
Leggio, M. G., Mandolesi, L., Federico, F., Spirito, F., Ricci, B., Gelfo, F., & Petrosini, L. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.04.009 · Cited by 502 · see citing works
Microglia in degenerative neurological disease
McGeer, P. L., Kawamata, T., Walker, D. G., Akiyama, H., Tooyama, I., & McGeer, E. G. (1993) · Glia · doi:10.1002/glia.440070114 · Cited by 500 · see citing works
Contribution of glial cells to the development of amyloid plaques in Alzheimer’s disease
Nagele, R. G., Węgiel, J., Venkataraman, V., Imaki, H., Wang, K.-C., & Wegiel, J. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.01.007 · Cited by 497 · see citing works
Microglia Biology in Health and Disease
Garden, G. A., & Möller, T. (2006) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-006-9015-5 · Cited by 494 · see citing works
Inflammatory processes in Alzheimer's disease
McGeer, E. G., & McGeer, P. L. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00124-6 · Cited by 473 · see citing works
The influence of age, gender, and race on the prevalence of depression in heart failure patients
Gottlieb, S. S., Khatta, M., Friedmann, E., Einbinder, L., Katzen, S. M., Baker, B., Marshall, J. P., Minshall, S., Robinson, S., Fisher, M. L., et al. (2004) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2003.10.064 · Cited by 468 · see citing works
Nieman, D. C., & Pedersen, B. K. (1999) · Sports Medicine · doi:10.2165/00007256-199927020-00001 · Cited by 466 · see citing works
Glial cell abnormalities in major psychiatric disorders: the evidence and implications
Cotter, D. R., Pariante, C. M., & Everall, I. P. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00527-5 · Cited by 465 · see citing works
Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice
Duman, C. H., Schlesinger, L., Russell, D. S., & Duman, R. S. (2008) · Brain Research · doi:10.1016/j.brainres.2007.12.047 · Cited by 465 · see citing works
Persistent and specific influences of early acoustic environments on primary auditory cortex
Zhang, L. I., Bao, S., & Merzenich, M. M. (2001) · Nature Neuroscience · doi:10.1038/nn745 · Cited by 450 · see citing works
Benaroya‐Milshtein, N., Hollander, N., Apter, A., Kukulansky, T., Raz, N., Wilf, A., Yaniv, I., & Pick, C. G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03587.x · Cited by 439 · see citing works
Socioeconomic status in childhood and the lifetime risk of major depression
Gilman, S. E., Kawachi, I. I., Fitzmaurice, G. M., & Buka, S. L. (2002) · International Journal of Epidemiology · doi:10.1093/ije/31.2.359 · Cited by 437 · see citing works
Kohut, M. L., McCann, D. A., Russell, D. W., Konopka, D. N., Cunnick, J. E., Franke, W. D., Castillo, M. C., Reighard, A. E., & Vanderah, E. (2006) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2005.12.002 · Cited by 436 · see citing works
Role of Serotonin in the Immune System and in Neuroimmune Interactions
Mößner, R., & Lesch, K. (1998) · Brain Behavior and Immunity · doi:10.1006/brbi.1998.0532 · Cited by 434 · see citing works
Microglial phenotype: is the commitment reversible?
Schwartz, M., Butovsky, O., Brück, W., & Hanisch, U.-K. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2005.12.005 · Cited by 434 · see citing works
Herz, R. S. (2009) · International Journal of Neuroscience · doi:10.1080/00207450802333953 · Cited by 418 · see citing works
The Role of Inflammation and Cytokines in Brain Injury
Arvin, B. M., Neville, L. F., Barone, F. C., & Feuerstein, G. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00026-7 · Cited by 417 · see citing works
Nutrition in Brain Development and Aging: Role of Essential Fatty Acids
Uauy, R. D., & Dangour, A. D. (2006) · Nutrition Reviews · doi:10.1301/nr.2006.may.s24-s33 · Cited by 417 · see citing works
BDNF release from single cells elicits local dendritic growth in nearby neurons
Horch, H. W., & Katz, L. C. (2002) · Nature Neuroscience · doi:10.1038/nn927 · Cited by 410 · see citing works
Neurodegenerative disease and adult neurogenesis
Winner, B., Kohl, Z., & Gage, F. H. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07613.x · Cited by 405 · see citing works
Mora, F., Segovia, G., & Arco, A. D. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.03.011 · Cited by 401 · see citing works
Regulation of hippocampal neurogenesis in adulthood
Gould, E., Tanapat, P., Rydel, T. A., & Hastings, N. B. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01021-0 · Cited by 400 · see citing works
Kuo, H., Yen, C., Chang, C., Kuo, C.-K., Chen, J.-H., & Sorond, F. A. (2005) · The Lancet Neurology · doi:10.1016/s1474-4422(05)70099-5 · Cited by 400 · see citing works
Licastro, F., Pedrini, S., Caputo, L., Annoni, G., Davis, L. J., Ferri, C., Casadei, V. M., & Grimaldi, L. M. E. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00226-x · Cited by 400 · see citing works
Improving housing conditions for laboratory mice: a review of 'environmental enrichment'
Olsson, I. A. S., & DAHLBORN, K. (2002) · Laboratory Animals · doi:10.1258/002367702320162379 · Cited by 395 · see citing works
Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms
Cassilhas, R. C., Lee, K. S., Fernandes, J., Oliveira, M. G. M., Tufik, S., Meeusen, R., & de Mello, M. T. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.029 · Cited by 394 · see citing works
Dilger, R. N., & Johnson, R. W. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.0208108 · Cited by 391 · see citing works
McKnight, J. R., Satterfield, M. C., Jobgen, W. S., Smith, S. B., Spencer, T. E., Meininger, C. J., McNeal, C. J., & Wu, G. (2010) · Amino Acids · doi:10.1007/s00726-010-0598-z · Cited by 376 · see citing works
Neuroprotective role of the innate immune system by microglia
Glezer, I., Simard, A. R., & Rivest, S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.055 · Cited by 371 · see citing works
The Leucocytosis of Exercise: A Review and Model
McCarthy, D. A., & Dale, M. M. (1988) · Sports Medicine · doi:10.2165/00007256-198806060-00002 · Cited by 370 · see citing works
Maratos, A., Gold, C., Wang, X., & Crawford, M. (2008) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004517.pub2 · Cited by 368 · see citing works
A review of environmental enrichment for pigs housed in intensive housing systems
de Weerd, H. A. V., & Day, J. E. L. (2008) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2008.08.001 · Cited by 358 · see citing works
Gates, N., Fiatarone Singh, M. A., Sachdev, P. S., & Valenzuela, M. (2013) · The American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2013.02.018 · Cited by 355 · see citing works
The role of IL-6 in mediating the anti-inflammatory effects of exercise.
Petersen, A. M. W., & Pedersen, B. K. (2006) · PubMed · Cited by 354 · see citing works
Kemper, K. J., & Danhauer, S. C. (2005) · Southern Medical Journal · doi:10.1097/01.smj.0000154773.11986.39 · Cited by 349 · see citing works
Dietary essential fatty acids and brain function: a developmental perspective on mechanisms
Wainwright, P. E. (2002) · Proceedings of the Nutrition Society · doi:10.1079/pns2001130 · Cited by 346 · see citing works
Molecular mechanisms involved in T cell migration across the blood–brain barrier
Engelhardt, B. (2006) · Journal of Neural Transmission · doi:10.1007/s00702-005-0409-y · Cited by 344 · see citing works
Conde, J. R., & Streit, W. J. (2006) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/01.jnen.0000202887.22082.63 · Cited by 344 · see citing works
Vitamin D and neurocognitive dysfunction: Preventing “D”ecline?
Buell, J. S., & Dawson‐Hughes, B. (2008) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2008.05.001 · Cited by 342 · see citing works
Dopamine, a neurotransmitter, influences the immune system
Basu, S., & Dasgupta, P. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00176-9 · Cited by 335 · see citing works
Microglia and Alzheimer's disease pathogenesis
Streit, W. J. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20093 · Cited by 335 · see citing works
Up-Regulated Production and Activation of the Complement System in Alzheimer's Disease Brain
Yasojima, K., Schwab, C., McGeer, E. G., & McGeer, P. L. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65340-0 · Cited by 328 · see citing works
Microglia Control Neuronal Network Excitability via BDNF Signalling
Ferrini, F., & Koninck, Y. D. (2013) · Neural Plasticity · doi:10.1155/2013/429815 · Cited by 321 · see citing works
Sensory stimulation as environmental enrichment for captive animals: A review
Wells, D. L. (2009) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.01.002 · Cited by 317 · see citing works
Dodel, R. C. (2004) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2003.033399 · Cited by 317 · see citing works
Ehninger, D. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.8.845 · Cited by 314 · see citing works
Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning
Buwalda, B., Kole, M. H. P., Veenema, A. H., Huininga, M., de Boer, S. F., Korte, S. M., & Koolhaas, J. M. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.05.005 · Cited by 304 · see citing works
Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice
Frick, K. M., & Fernandez, S. M. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00138-0 · Cited by 303 · see citing works
Laviola, G., Hannan, A. J., Macrì, S., Solinas, M., & Jaber, M. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.05.001 · Cited by 300 · see citing works
Drollette, E. S., Scudder, M. R., Raine, L. B., Moore, R. D., Saliba, B. J., Pontifex, M. B., & Hillman, C. H. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2013.11.001 · Cited by 298 · see citing works
Brain-Derived Neurotrophic Factor Enhances Long-Term Potentiation in Rat Visual Cortex
Akaneya, Y., Tsumoto, T., Kinoshita, S., & Hatanaka, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-17-06707.1997 · Cited by 284 · see citing works
Astrocytes: Form, Functions, and Roles in Disease
Montgomery, D. L. (1994) · Veterinary Pathology · doi:10.1177/030098589403100201 · Cited by 279 · see citing works
Acceleration of Visual System Development by Environmental Enrichment
Cancedda, L., Putignano, E., Sale, A., Viegi, A., Berardi, N., & Maffei, L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0845-04.2004 · Cited by 278 · see citing works
Social environment is associated with gene regulatory variation in the rhesus macaque immune system
Tung, J., Barreiro, L. B., Johnson, Z. P., Hansen, K. D., Michopoulos, V., Toufexis, D., Michelini, K., Wilson, M. E., & Gilad, Y. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202734109 · Cited by 277 · see citing works
Ruis, M. A. W., Brake, J. H. A. T., Buwalda, B., de Boer, S. F., Meerlo, P., Korte, S. M., Blokhuis, H. J., & Koolhaas, J. M. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00050-x · Cited by 275 · see citing works
Omega-3 fatty acids and rodent behavior
Fedorova, I., & Salem, N. (2006) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2006.07.006 · Cited by 274 · see citing works
Effects of a Music Therapy Strategy on Depressed Older Adults
Hanser, S. B., & Thompson, L. W. (1994) · Journal of Gerontology · doi:10.1093/geronj/49.6.p265 · Cited by 266 · see citing works
Nutrition, Brain Aging, and Neurodegeneration: Table 1.
Joseph, J., Cole, G., Head, E., & Ingram, D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3520-09.2009 · Cited by 264 · see citing works
Pham, T. M., Ickes, B. R., Albeck, D. S., Söderström, S., Granholm, A.-C., & Mohammed, A. H. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00316-4 · Cited by 262 · see citing works
Baumans, V. (2005) · ILAR Journal · doi:10.1093/ilar.46.2.162 · Cited by 260 · see citing works
Microglia and neuroprotection: implications for Alzheimer's disease
Streit, W. J. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.013 · Cited by 256 · see citing works
Exercise and Toll-like receptors
Gleeson, M., McFarlin, B. K., & Flynn, M. G. (2026) · PubMed · doi:10.22029/eir.2006.1621 · Cited by 254 · see citing works
NT-3 and/or BDNF therapy prevents loss of auditory neurons following loss of hair cells
Staecker, H., Kopke, R. D., Malgrange, B., Lefebvre, P. P., & Water, T. R. V. D. (1996) · Neuroreport · doi:10.1097/00001756-199603220-00011 · Cited by 252 · see citing works
Marashi, V., Barnekow, A., Ossendorf, E., & Sachser, N. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00002-3 · Cited by 250 · see citing works
Response of the brain to enrichment
Diamond, M. C. (2001) · Anais da Academia Brasileira de Ciências · doi:10.1590/s0001-37652001000200006 · Cited by 246 · see citing works
Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism
Faherty, C. J., Shepherd, K. R., Herasimtschuk, A., & Smeyne, R. J. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.08.008 · Cited by 241 · see citing works
Hannan, A. J. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12102 · Cited by 240 · see citing works
B cell exchange across the blood-brain barrier in multiple sclerosis
von Büdingen, H. ‐., Kuo, T. C., Sirota, M., van Belle, C. J., Apeltsin, L., Glanville, J., Cree, B., Gourraud, P., Schwartzburg, A., Huerta, G., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci63842 · Cited by 239 · see citing works
Cytokines and their receptors in the central nervous system: Physiology, pharmacology, and pathology
Rothwell, N. J., Luheshi, G., & Toulmond, S. (1996) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(95)02033-0 · Cited by 233 · see citing works
van der Borght, K., Havekes, R., Bos, T., Eggen, B. J. L., & van der Zee, E. A. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.324 · Cited by 227 · see citing works
Lees, C., & Hopkins, J. (2013) · Preventing Chronic Disease · doi:10.5888/pcd10.130010 · Cited by 226 · see citing works
T-helper-1 and T-helper-2 Responses in Psychiatric Disorders
Schwarz, M., Chiang, S. S. W., Müller, N., & Ackenheil, M. (2001) · Brain Behavior and Immunity · doi:10.1006/brbi.2001.0647 · Cited by 220 · see citing works
Cerebral pattern of pro- and anti-inflammatory cytokines in dementias
Tarkowski, E., Liljeroth, A.-M., Minthon, L., Tarkowski, A., Wallin, A., & Blennow, K. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(03)00088-1 · Cited by 219 · see citing works
Schaller, M., Miller, G. E., Gervais, W. M., Yager, S., & Chen, E. (2010) · Psychological Science · doi:10.1177/0956797610368064 · Cited by 219 · see citing works
Carmignoto, G., Pizzorusso, T., Tia, S., & Vicini, S. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp021848 · Cited by 219 · see citing works
Acute phase proteins in major depression
Berk, M., Wadee, A. A., Kuschke, R. H., & O’Neill-Kerr, A. (1997) · Journal of Psychosomatic Research · doi:10.1016/s0022-3999(97)00139-6 · Cited by 215 · see citing works
Social status in mice: behavioral, endocrine and immune changes are context dependent
Bartolomucci, A., Palanza, P., Gaspani, L., Limiroli, E., Panerai, A. E., Ceresini, G., Poli, M., & Parmigiani, S. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00453-x · Cited by 214 · see citing works
Cytokines and adhesion molecules in stroke and related diseases
Kim, J. S. (1996) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(95)00338-3 · Cited by 213 · see citing works
Exercise improves cognition and hippocampal plasticity in <i>APOE</i> ɛ4 mice
Nichol, K., Deeny, S. P., Seif, J., Camaclang, K., & Cotman, C. W. (2009) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2009.02.006 · Cited by 213 · see citing works
Beneficial effects of exercise and its molecular mechanisms on depression in rats.
Zheng, H., Liu, Y., Li, W., Yang, B., Chen, D., Wang, X., Jiang, Z., Wang, H., Wang, Z., Cornelisson, G., et al. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.10.007 · Cited by 212 · see citing works
Neuroinflammation and Cognitive Aging
Ownby, R. L. (2010) · Current Psychiatry Reports · doi:10.1007/s11920-009-0082-1 · Cited by 212 · see citing works
Experience facilitates olfactory quality discrimination
Rabin, M. D. (1988) · Perception & Psychophysics · doi:10.3758/bf03207487 · Cited by 211 · see citing works
Navarro, A., Gómez, C., Sánchez-Pino, M.-J., González, H., Bández, M. J., Boveris, A. D., & Boveris, A. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00834.2004 · Cited by 209 · see citing works
Fernández‐Teruel, A., Escorihuela, R. M., Castellano, B., González, B., & Tobeña, A. (1997) · Behavior Genetics · doi:10.1023/a:1021400830503 · Cited by 207 · see citing works
Chapillon, P., Patin, V., Roy, V., Vincent, A., & Caston, J. (2002) · Developmental Psychobiology · doi:10.1002/dev.10066 · Cited by 206 · see citing works
Cognitive stimulation of patients with dementia: Preliminary results
Breuil, V., de Rotrou, J., Forette, F., Tortrat, D., Ganansia‐Ganem, A., Frambourt, A., Moulin, F., & Boller, F. (1994) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.930090306 · Cited by 204 · see citing works
Trollor, J. N., Smith, E., Agars, E., Kuan, S. A., Baune, B. T., Campbell, L. V., Samaras, K., Crawford, J., Lux, O., Kochan, N. A., et al. (2011) · AGE · doi:10.1007/s11357-011-9301-x · Cited by 204 · see citing works
Self-citationPassineau, M. J., Green, E. J., & Dietrich, W. D. (2001) · Experimental Neurology · doi:10.1006/exnr.2000.7623 · Cited by 204 · see citing works
Experience induces structural and biochemical changes in the adult primate brain
Kozorovitskiy, Y., Gross, C. G., Kopil, C., Battaglia, L., McBreen, M., Stranahan, A. M., & Gould, E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508817102 · Cited by 202 · see citing works
Engineer, N. D., Percaccio, C. R., Pandya, P. K., Moucha, R., Rathbun, D. L., & Kilgard, M. P. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00059.2004 · Cited by 198 · see citing works
BENNETT, J., McRae, P. A., Levy, L. J., & Frick, K. M. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.09.003 · Cited by 198 · see citing works
Reduced Olfactory Bulb Volume in Patients With Schizophrenia
Turetsky, B. I., Moberg, P. J., Yousem, D. M., Doty, R. L., Arnold, S. E., & Gur, R. E. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.5.828 · Cited by 197 · see citing works
Environmental enrichment: Effects on spatial memory and hippocampal CREB immunoreactivity
Williams, B. M., Luo, Y. M., Ward, C. P., Redd, K. J., Gibson, R., Kuczaj, S. A., & McCoy, J. G. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00543-1 · Cited by 191 · see citing works
Strait, D. L., & Kraus, N. (2013) · Hearing Research · doi:10.1016/j.heares.2013.08.004 · Cited by 191 · see citing works
Olfaction in infants and children: developmental and functional perspectives
Schaal, B. (1988) · Chemical Senses · doi:10.1093/chemse/13.2.145 · Cited by 190 · see citing works
Marais, L., Stein, D. J., & Daniels, W. M. U. (2009) · Metabolic Brain Disease · doi:10.1007/s11011-009-9157-2 · Cited by 190 · see citing works
Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice
Binder, E., Droste, S. K., Ohl, F., & Reul, J. M. H. M. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.04.017 · Cited by 188 · see citing works
Neuroimmunological effects of physical exercise in depression
Eyre, H. A., & Baune, B. T. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.09.015 · Cited by 188 · see citing works
Self-citationSpeisman, R. B., Kumar, A., Rani, A., Foster, T. C., & Ormerod, B. K. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.013 · Cited by 187 · see citing works
Trøseid, M. (2004) · European Heart Journal · doi:10.1016/j.ehj.2003.12.006 · Cited by 187 · see citing works
Environmental influences on brain neurotrophins in rats
Pham, T. M., Winblad, B. G., Granholm, A., & Mohammed, A. H. S. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00783-9 · Cited by 184 · see citing works
Torasdotter, M., METSIS, M. L., Henriksson, B. G., Winblad, B. G., & Mohammed, A. H. S. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00142-3 · Cited by 184 · see citing works
The role of chemokines in inflammation
Proost, P., Wuyts, A., & Damme, J. V. (1996) · International Journal of Clinical & Laboratory Research · doi:10.1007/bf02602952 · Cited by 182 · see citing works
Tooyama, I., Kimura, H., Akiyama, H., & McGeer, P. L. (1990) · Brain Research · doi:10.1016/0006-8993(90)91496-4 · Cited by 180 · see citing works
Preferences for nesting material as environmental enrichment for laboratory mice
de Weerd, H. A. V., Loo, P. L. P. V., van Zutphen, L. F. M., Koolhaas, J. M., & Baumans, V. (1997) · Laboratory Animals · doi:10.1258/002367797780600152 · Cited by 179 · see citing works
Beauquis, J., Pavía, P., Pomilio, C. J., Vinuesa, Á., Podlutskaya, N., Galván, V., & Saravia, F. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.09.009 · Cited by 177 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Fuglestad A. J. Rao R. Georgieff M. K. Code M. M. (2008). “The role of nutrition in cognitive development,” in Handbook in Developmental Cognitive Neuroscience 2nd Edn eds Nelson C. A. Luciana M. (Cambridge, MA: MIT Press) 623– 642
Cited by
Sorted by citations
Microglia in physiology and disease
Wolf, S. A., Boddeke, H. W. G. M., & Kettenmann, H. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034406 · Cited by 1,426 · see citing works
The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology
Rutsch, A., Kantsjö, J. B., & Ronchi, F. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604179 · Cited by 821 · see citing works
Wellman, C. L., Bangasser, D. A., Bollinger, J. L., Coutellier, L., Logrip, M. L., Moench, K. M., & Urban, K. R. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1673-18.2018 · Cited by 88 · see citing works
Regulation of astrocyte metabolism by mitochondrial translocator protein <scp>18 kDa</scp>
Firth, W., Robb, J. L., Stewart, D., Pye, K. R., Bamford, R., Oguro‐Ando, A., Beall, C., & Ellacott, K. L. J. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16089 · Cited by 5 · see citing works
- Authors
- Singhal, G., Jaehne, E. J., Corrigan, F., & Baune, B. T.
- Affiliations
- The University of Adelaide (AU)
- Corresponding author
- Baune, Bernhard T.
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2014-04-03
- Volume
- 8
- Pages
- 97-97
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC3982075
- OpenAlex
- W2029961705
- Cited by
- 186
- References
- 346
- Citations by year
- 2026: 10 · 2025: 16 · 2024: 20 · 2023: 18 · 2022: 16 · 2021: 19 · 2020: 29 · 2019: 12 · 2018: 12 · 2017: 10 · 2016: 12 · 2015: 9 · 2014: 2 · 2013: 1
- FWCI
- 0.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Funders
- Medical Research Council
- National Health and Medical Research Council (1043771)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- environmental enrichment, neuroimmunomodulation, physical activity, cytokines, interleukin-6, Toll-like receptors, adipokines, microglia, T cells, natural killer cells, social defeat, sensory enrichment, IL-1β, TNF-α, IL-10, mental illness
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review