The DOI matches its Crossref record; 346 of the 346 references it cites were found in a registry or an index.
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.
Overview
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
Verification
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?
In the citing paper
“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.
Citations
Cites
Items 201–346 of 346
(2001) · PubMed · Cited by 175
Corotto, F. S., Henegar, J. R., & MARUNIAK, J. A. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90397-2 · Cited by 174
Gobbo, O. L., & O’Mara, S. M. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.10.017 · Cited by 174
Exercise, Training and Neutrophil Microbicidal Activity
Smith, J., Telford, R. D., Mason, I., & Weidemann, M. J. (1990) · International Journal of Sports Medicine · doi:10.1055/s-2007-1024788 · Cited by 174
Cognitive dysfunction in mice deficient for TNF‐ and its receptors
Baune, B. T., Wiede, F., Braun, A., Golledge, J., Arolt, V., & Körner, H. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30712 · Cited by 173
Self-citationInflammation, the complement system and the diseases of aging
McGeer, E. G., Klegeris, A., & McGeer, P. L. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.08.008 · Cited by 170
Effects of Environmental Enrichment on Spatial Memory and Neurochemistry in Middle-Aged MicePreprint
Frick, K. M., Stearns, N. A., Pan, J.-Y., & Berger-Sweeney, J. E. (2003) · Learning & Memory · doi:10.1101/lm.50703 · Cited by 170
Exercise enhances hippocampal‐dependent learning in the rat: Evidence for a BDNF‐related mechanism
Griffin, É. W., Bechara, R. G., Birch, A. M., & Kelly, A. M. (2009) · Hippocampus · doi:10.1002/hipo.20631 · Cited by 168
Hamm, R. J., Temple, M. D., O’Dell, D. M., PIKE, B. R., & Lyeth, B. G. (1996) · Journal of Neurotrauma · doi:10.1089/neu.1996.13.41 · Cited by 168
High Intensity Exercise: A Cause of Lymphocyte Apoptosis?
Mars, M., Govender, S., Weston, A. R., Naicker, V. L., & Chuturgoon, A. A. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9156 · Cited by 166
Inflammation, Neurodegenerative Diseases, and Environmental Exposures
Campbell, A. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1332.008 · Cited by 166
The complement system and innate immunity
Janeway, C. A., Travers, P. J., Walport, M. J., & Shlomchik, M. J. (2001) · Cited by 165
Immune changes in humans during cold exposure: effects of prior heating and exercise
Brenner, I., Castellani, J. W., Gabaree, C. L. V., Young, A., Zamecnik, J., Shephard, R. J., & Shek, P. N. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.2.699 · Cited by 164
Tha, K. K., Okuma, Y., Miyazaki, H., Murayama, T., Uehara, T., Hatakeyama, R., Hayashi, Y., & Nomura, Y. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02883-3 · Cited by 163
Pham, T. M., Söderström, S., Winblad, B., & Mohammed, A. H. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00019-4 · Cited by 162
Chemokines and neuromodulation
Parsadaniantz, S. M., & Rostène, W. H. (2008) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.04.022 · Cited by 162
Kobayashi, S., Ohashi, Y., & Ando, S. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10442 · Cited by 156
Beneficial effects of enriched environment on adolescent rats from stressed pregnancies.
Laviola, G., Rea, M., Morley‐Fletcher, S., Di Carlo, S., Bacosi, A., De Simone, R., Bertini, M., & Pacifici, R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03597.x · Cited by 155
The effect of environmental enrichment on the behaviour of caged rabbits (Oryctolagus cuniculus)
Hansen, L. T., & Berthelsen, H. (2000) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(00)00093-9 · Cited by 154
Treating Depression and Depression-Like Behavior with Physical Activity: An Immune Perspective
Eyre, H. A., Papps, E., & Baune, B. T. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00003 · Cited by 153
Self-citationInfluence of Dinner Music on Food Intake and Symptoms Common in Dementia
Ragneskog, H., Bråne, G., Karlsson, I., & Kihlgren, M. (1996) · Scandinavian Journal of Caring Sciences · doi:10.1111/j.1471-6712.1996.tb00304.x · Cited by 152
A unique role for the human amygdala in novelty detection
Blackford, J. U., Buckholtz, J. W., Avery, S. N., & Zald, D. H. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.083 · Cited by 152
Prenatal Stress Depresses Immune Function in Rats
Kay, G., Tarcic, N., Poltyrev, T., & Weinstock, M. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00456-3 · Cited by 149
Beauquis, J., Pavía, P., Pomilio, C., Vinuesa, A., Podlutskaya, N., Galvan, V., & Saravia, F. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2012.09.009 · Cited by 148
Williamson, L. L., Chao, A. S., & Bilbo, S. D. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.01.003 · Cited by 147
Chemokines are elevated in plasma after strenuous exercise in humans
Ostrowski, K., Rohde, T., Asp, S., Schjerling, P., & Pedersen, B. K. (2001) · European Journal of Applied Physiology · doi:10.1007/s004210170012 · Cited by 146
Stress and the aging immune system
Hawkley, L. C., & Cacioppo, J. T. (2003) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2003.09.005 · Cited by 146
Keeney, A. J., & Hogg, S. L. (1999) · Behavioural Pharmacology · doi:10.1097/00008877-199912000-00007 · Cited by 144
Influence of cage enrichment on aggressive behaviour and physiological parameters in male mice
Loo, P. L. P. V., Kruitwagen, C. L. J. J., Koolhaas, J. M., de Weerd, H. A. V., van Zutphen, L. F. M., & Baumans, V. (2002) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(01)00200-3 · Cited by 140
Is the anti-inflammatory effect of regular exercise responsible for reduced cardiovascular disease?
Wilund, K. R. (2007) · Clinical Science · doi:10.1042/cs20060368 · Cited by 138
Neurobiology of early life stress: Rodent studies
Gutman, D. A., & Nemeroff, C. B. (2002) · Seminars in Clinical Neuropsychiatry · doi:10.1053/scnp.2002.31781 · Cited by 137
Möckel, M., Röcker, L., Störk, T., Vollert, J., Danne, O., Eichstädt, H., Müller, R., & Hochrein, H. (1994) · European Journal of Applied Physiology and Occupational Physiology · doi:10.1007/bf00599512 · Cited by 137
Behavioural and glial changes in old rats following environmental enrichment.
Soffié, M., Hahn, K., Terao, E., & Eclancher, F. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00139-9 · Cited by 136
Bowie, C. R., Gupta, M., Holshausen, K., Jokic, R., Best, M., & Milev, R. (2013) · Journal of Nervous & Mental Disease · doi:10.1097/nmd.0b013e31829c5030 · Cited by 136
Music interventions for people with dementia: a review of the literature
Sherratt, K., Thornton, A., & Hatton, C. (2004) · Aging & Mental Health · doi:10.1080/13607860310001613275 · Cited by 135
The Effect of Music on Cognitive Performance: Insight From Neurobiological and Animal Studies
Rickard, N. S., Toukhsati, S. R., & Field, S. E. (2005) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582305285869 · Cited by 134
Blue Light Stimulates Cognitive Brain Activity in Visually Blind Individuals
Vandewalle, G., Collignon, O., Hull, J. T., Daneault, V., Albouy, G., Leporé, F., Phillips, C. L. M., Doyon, J., Czeisler, C. A., Dumont, M., et al. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00450 · Cited by 133
Xie, Z. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00057-8 · Cited by 133
Effect of music-based multitask training on cognition and mood in older adults
Hars, M., Herrmann, F. R., Gold, G., Rizzoli, R., & Trombetti, A. (2013) · Age and Ageing · doi:10.1093/ageing/aft163 · Cited by 133
Mental health implications of music: insight from neuroscientific and clinical studies.
Lin, S.-T., Yang, P.-C., Lai, C., Su, Y.-Y., Yeh, Y.-C., Huang, M.-F., & Chen, C.-C. (2011) · Harvard Review of Psychiatry · doi:10.3109/10673229.2011.549769 · Cited by 132
Effects of music therapy on depression compared with psychotherapy
Castillo-Pérez, S., Gómez-Pérez, V., Velasco, M. C., Pérez‐Campos, E., & Mayoral, M. Á. (2010) · The Arts in Psychotherapy · doi:10.1016/j.aip.2010.07.001 · Cited by 132
The effects of different types of music on mood, tension, and mental clarity.
McCraty, R., Barrios-Choplin, B., Atkinson, M., et al. (1998) · PubMed · Cited by 129
Bogoch, S. (1969) · Springer eBooks · doi:10.1007/978-1-4899-6323-9_29 · Cited by 128
Effect of Resistance Exercise on Serum Levels of Growth Factors in Humans
Vega, S. R., Knicker, A. J., Hollmann, W., Bloch, W., & Strüder, H. K. (2010) · Hormone and Metabolic Research · doi:10.1055/s-0030-1267950 · Cited by 127
Dominant–submissive behavior as models of mania and depression
Malatyńska, E., & Knapp, R. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.014 · Cited by 125
Fan, Y., Liu, Z., Weinstein, P. R., Fike, J. R., & Liu, J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05269.x · Cited by 124
Social stress and the regulation of tumor necrosis factor-α secretion
Avitsur, R., Kavelaars, A., Heijnen, C. J., & Sheridan, J. F. (2004) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2004.09.005 · Cited by 124
Angelucci, F., Ricci, E., Padua, L., Sabino, A., & Tonali, P. A. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.10.005 · Cited by 120
Reduced serum antibodies associated with social defeat in rats
Fleshner, M., Laudenslager, M. L., Simons, L., & Maier, S. F. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90107-8 · Cited by 119
Effects of acute and chronic social stress on blood cellular immunity in rats
Stefanski, V., & Engler, H. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00127-9 · Cited by 119
Ma, X., Jiang, D., Jiang, W., Wang, F., Jia, M., Wu, J., Hashimoto, K., Dang, Y., & Gao, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020955 · Cited by 118
Age-changes of brain synapses and synaptic plasticity in response to an enriched environment
Nakamura, H., Kobayashi, S., Ohashi, Y., & Ando, S. (1999) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19990501)56:3 · Cited by 118
Preference for social contact versus environmental enrichment in male laboratory mice
Van Loo, P. L. P., Van de Weerd, H. A., Van Zutphen, L. F. M., & Baumans, V. (2004) · Laboratory Animals · doi:10.1258/002367704322968867 · Cited by 118
Alzheimer disease and neuroinflammation
McGeer, P. L., McGeer, E. G., & Yasojima, K. (2000) · Springer eBooks · doi:10.1007/978-3-7091-6781-6_8 · Cited by 117
Strength of preference 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. (1998) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(97)00043-9 · Cited by 116
NK Cells in Central Nervous System Disorders
Poli, A., Kmiecik, J., Domingues, O., Hentges, F., Bléry, M., Chekenya, M., Boucraut, J., & Zimmer, J. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1203401 · Cited by 115
Exercise normalises overexpression of TNF-α in knockout mice
Keller, C., Keller, P., Giralt, M., Hidalgo, J., & Pedersen, B. K. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.06.129 · Cited by 114
Olfactory experience modulates apoptosis in the developing olfactory bulb
Najbauer, J., & Leon, M. (1995) · Brain Research · doi:10.1016/0006-8993(94)01448-q · Cited by 113
Berardi, N., Braschi, C., Capsoni, S., Cattaneo, A., & Maffei, L. (2007) · Journal of Alzheimer s Disease · doi:10.3233/jad-2007-11312 · Cited by 110
Vitamins B12, B6, and folic acid for cognition in older men
Ford, A., Flicker, L., Alfonso, H., Thomas, J., Clarnette, R., Martins, R. N., & Almeida, O. (2010) · Neurology · doi:10.1212/wnl.0b013e3181f962c4 · Cited by 109
Tvede, N., Pedersen, B. K., HANSEN, F. R., Bendix, T., Christensen, L., Galbo, H., & Halkjær-Kristensen, J. (1989) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.1989.tb01137.x · Cited by 109
Papaioannou, A., Gerozissis, K., Prokopiou, A., Bolaris, S., & Stylianopoulou, F. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00334-5 · Cited by 107
To smell the immune system: Olfaction, autoimmunity and brain involvement
Strous, R. D., & Shoenfeld, Y. (2006) · Autoimmunity Reviews · doi:10.1016/j.autrev.2006.07.002 · Cited by 106
Veyrac, A., Sacquet, J., Nguyen, V., Marien, M. R., Jourdan, F., & Didier, A. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.191 · Cited by 105
Neurobiological effects of neonatal maternal separation and post-weaning environmental enrichment.
Vivinetto, A. L., Suárez, M. M., & Rivarola, M. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.11.014 · Cited by 103
Local Effects of BDNF on Dendritic Growth
Horch, H. W. (2004) · Reviews in the Neurosciences · doi:10.1515/revneuro.2004.15.2.117 · Cited by 103
Preferences of mice and rats for types of bedding material
Blom, H. J. M., van Tintelen, G., van Vorstenbosch, C. J. A. H. V., Baumans, V., & Beynen, A. C. (1996) · Laboratory Animals · doi:10.1258/002367796780684890 · Cited by 103
Chikahisa, S., Séi, H., Morishima, M., Sano, A., Kitaoka, K., Nakaya, Y., & Morita, Y. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.01.021 · Cited by 100
Welberg, L., Thrivikraman, K. V., & Plotsky, P. M. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.11.011 · Cited by 98
Lymphocytes and NK cell activity during repeated bouts of maximal exercise
Nielsen, H. B., Secher, N. H., Christensen, N. J., & Pedersen, B. K. (1996) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1996.271.1.r222 · Cited by 97
Effect of the environment on the dendritic morphology of the rat auditory cortex
Bose, M., Muñoz-LLancao, P., Roychowdhury, S., Nichols, J., Jakkamsetti, V., Porter, B. A., Byrapureddy, R., Salgado, H., Kilgard, M. P., Aboitiz, F., et al. (2009) · Synapse · doi:10.1002/syn.20710 · Cited by 97
Arranz, L., Castro, N. M. D., Baeza, I., Maté, I., Viveros, M., & la Fuente, M. D. (2010) · Rejuvenation Research · doi:10.1089/rej.2009.0989 · Cited by 96
Environmental enrichment stimulates progenitor cell proliferation in the amygdala
Okuda, H., Tatsumi, K., Makinodan, M., Yamauchi, T., Kishimoto, T., & Wanaka, A. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22160 · Cited by 96
Jurgens, H. A., & Johnson, R. W. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.05.015 · Cited by 95
Attention and memory in aged rats: Impact of lifelong environmental enrichment.
Harati, H., Majchrzak, M., Cosquer, B., Galani, R., Kelche, C., Cassel, J., & Barbelivien, A. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.03.012 · Cited by 94
Roberts, J. E. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05408.x · Cited by 93
Immunological outcomes of exercise in older adults
Senchina, D. S., & Kohut, M. L. (2007) · Clinical Interventions in Aging · doi:10.2147/ciia.2007.2.1.3 · Cited by 91
Effect of a Computerized Brain Exercise Program on Cognitive Performance in Older Adults
Miller, K. J., Dye, R. V., Kim, J., Jennings, J. L., O'Toole, E., Wong, J., & Siddarth, P. (2013) · The American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2013.01.077 · Cited by 90
Social stress in laboratory rats
Stefanski, V. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00495-4 · Cited by 90
Angelucci, F., Fiore, M., Ricci, E., et al. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282d28f50 · Cited by 88
Bilbo, S. D., Newsum, N. J., Sprunger, D. B., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.10.005 · Cited by 88
Angelucci, F., Bartolo, P. D., Gelfo, F., Foti, F., Cutuli, D., Bossù, P., Caltagirone, C., & Petrosini, L. (2009) · The Cerebellum · doi:10.1007/s12311-009-0129-1 · Cited by 88
Bock, J., Murmu, M. S., Biala, Y., Weinstock, M., & Braun, K. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.048 · Cited by 86
Prenatal Immune Challenge Affects Growth, Behavior, and Brain Dopamine in Offspring
Bakoš, J., Dunčko, R., Makatsori, A., Pirník, Z., Kiss, A., & Ježová, D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.033 · Cited by 85
Effects of environmental enrichment on males of a docile inbred strain of mice
Marashi, V., Barnekow, A., & Sachser, N. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.05.009 · Cited by 84
Manjunatha, S. (2013) · JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH · doi:10.7860/jcdr/2013/5855.3341 · Cited by 84
Social stress, dominance and blood cellular immunity
Stefanski, V., & Engler, H. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(98)00242-2 · Cited by 79
Social environment determines the long-term effects of social defeat
de Jong, J. G., van der Vegt, B. J., Buwalda, B., & Koolhaas, J. M. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.10.013 · Cited by 79
Stimulation of the phagocytic function of neutrophils in sedentary men after acute moderate exercise
Ortega, E., Collazos, M. E., Maynar-Mariño, M., Barriga, C., & la Fuente, M. D. (1993) · European Journal of Applied Physiology · doi:10.1007/bf00863401 · Cited by 78
Núñez, M. J., Mañá, P., Liñares, D., Riveiro, M. P., Balboa, J., Suárez-Quintanilla, J., Maracchi, M., Méndez, M. R., López, J. M., & Freire-Garabal, M. (2002) · Life Sciences · doi:10.1016/s0024-3205(02)01796-4 · Cited by 78
TH1/TH2 CYTOKINES IN THE CENTRAL NERVOUS SYSTEM
Sredni, D. (2002) · International Journal of Neuroscience · doi:10.1080/00207450290025725 · Cited by 76
Arakawa, H., Arakawa, K., & Terrence Deak, B. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.01.002 · Cited by 74
Felten, D. L. (2008) · Neuropsychobiology · doi:10.1159/000119011 · Cited by 71
Tuan, T., Hsu, T.-G., Fong, M.-C., Hsu, C. C. S., Tsai, K. K., Lee, C.-Y., & Kong, C.-W. (2007) · British Journal of Sports Medicine · doi:10.1136/bjsm.2006.029314 · Cited by 71
Tumor Necrosis Factor Gene Variation Predicts Hippocampus Volume in Healthy Individuals
Baune, B. T., Konrad, C., Grotegerd, D., Suslow, T., Ohrmann, P., Bauer, J., Arolt, V., Heindel, W. L., Domschke, K., Schöning, S., et al. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.002 · Cited by 68
Self-citationVitamins and Cognition: What is the Evidence?
Kennedy, D. O., & Haskell, C. F. (2011) · Drugs · doi:10.2165/11594130-000000000-00000 · Cited by 67
Exercise suppresses macrophage antigen presentation
Ceddia, M. A., & Woods, J. A. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.6.2253 · Cited by 66
Roberts, J. E. (1995) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/1011-1344(95)90241-4 · Cited by 65
Sampedro‐Piquero, P., Zancada-Menéndez, C., Begega, A., Rubio, S., & Arias, J. L. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.06.006 · Cited by 60
Wainwright, P. E., Huang, Y. S., Bulman‐Fleming, B., Lévesque, S., & McCutcheon, D. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90139-2 · Cited by 59
Xu, J., Yu, L., Cai, R., Zhang, J., & Sun, X. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.07.018 · Cited by 59
A study of behavioural responses of non-human primates to air transport and re-housing
Honess, P. E., Johnson, P. J., & Wolfensohn, S. (2004) · Laboratory Animals · doi:10.1258/002367704322968795 · Cited by 59
Tees, R. C. (1999) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199912)35:4 · Cited by 57
Cai, R., Guo, F., Zhang, J., Xu, J., Cui, Y., & Sun, X. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.01.005 · Cited by 56
Ortega, E., Giraldo, E., Hinchado, M. D., Martín-Cordero, L., García, J. J., & la Fuente, M. D. (2007) · NeuroImmunoModulation · doi:10.1159/000110648 · Cited by 55
Altered T-lymphocyte response following aggressive encounters in mice
Hardy, C.-A., Quay, J., Livnat, S., et al. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90378-h · Cited by 53
Preferences for Nest Boxes 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. (1998) · Animal Welfare · doi:10.1017/s0962728600020224 · Cited by 53
Environmental enrichment enhances auditory takeover of the occipital cortex in anophthalmic mice
Piché, M., Robert, S., Miceli, D., & Bronchti, G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03823.x · Cited by 52
Rat C‐reactive protein activates the autologous complement system
Padilla, N. D., Bleeker, W. K., Lubbers, Y. T. P., Rigter, G. M. M., van Mierlo, G. J., Daha, M. R., & Hack, C. E. (2003) · Immunology · doi:10.1046/j.1365-2567.2003.01681.x · Cited by 51
Nutrition and development: other micronutrients' effect on growth and cognition.
Wasantwisut, E. (1997) · PubMed · Cited by 50
Rosselli-Austin, L., & Williams, J. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90267-3 · Cited by 49
Cage colour preferences and effects of home cage colour on anxiety in laboratory mice
Sherwin, C. M., & Glen, E. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2286 · Cited by 49
Aging and immune response to exercise
Shinkai, S., Konishi, M., & Shephard, R. J. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-76-5-562 · Cited by 48
Immune responses to inflammation and trauma: a physical training model
Shephard, R. J., & Shek, P. N. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-76-5-469 · Cited by 46
Exercise-induced enhancement of immune function in the rat.
Kaufman, J., Harris, T. J., Higgins, J., et al. (1994) · Circulation · doi:10.1161/01.cir.90.1.525 · Cited by 46
Shupak, A., & Gilbey, P. (2008) · Elsevier eBooks · doi:10.1016/b978-1-4160-3406-3.50027-5 · Cited by 46
The material culture of homicidal fantasies
Crabb, P. B. (2000) · Aggressive Behavior · doi:10.1002/(sici)1098-2337(2000)26:3 · Cited by 45
Venable, N., Fernández, V., Dı́az, E., & Pinto‐Hamuy, T. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90068-0 · Cited by 43
Effect of exercise on learning, memory and levels of epinephrine in rats' hippocampus.
Ahmadiasl, N., Alaei, H., & Hänninen, O. (2003) · Europe PMC (PubMed Central) · Cited by 41
Batzina, A., Dalla, C., Papadopoulou‐Daifoti, Z., & Karakatsouli, N. (2013) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2013.12.001 · Cited by 40
A single social defeat transiently suppresses the anti-viral immune response in mice
de Groot, J., van Milligen, F. J., Moonen-Leusen, B., Thomas, G., & Koolhaas, J. M. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00005-3 · Cited by 39
Licastro, F. (2003) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(03)00034-4 · Cited by 38
Social stress paradigms in male mice: Variations in behavior, stress and immunology
Fano, E., Sánchez‐Martín, J. R., Arregi, A., et al. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00445-0 · Cited by 38
Ron‐Harel, N., Cardon, M., & Schwartz, M. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.12.011 · Cited by 37
The role of IL-6 572 C/G, 190 C/T, and 174 G/C gene polymorphisms in children’s obesity
Oana, M. C., Bănescu, C. V., Duicu, C., Maria, P. A., Voidăzan, S. T., & Mărginean, C. (2014) · European Journal of Pediatrics · doi:10.1007/s00431-014-2315-5 · Cited by 37
Relations between aggressive behavior, immune activity, and disease susceptibility
Azpiroz, A., Garmendia, L., Fano, E., & Sánchez‐Martín, J. R. (2003) · Aggression and Violent Behavior · doi:10.1016/s1359-1789(02)00066-6 · Cited by 33
Jakkamsetti, V., Chang, K. Q., & Kilgard, M. P. (2011) · Journal of Neurophysiology · doi:10.1152/jn.01057.2010 · Cited by 32
Cellular responses to moderate and heavy exercise
Nehlsen‐Cannarella, S. L. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-76-5-485 · Cited by 30
Endocrine and lymphoproliferative response changes produced by social stress in mice
Cacho, R., Fano, E., Areso, P., Garmendia, L., Vegas, Ó., Brain, P. F., & Azpiroz, A. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00018-0 · Cited by 29
Anomal, R. F., de Villers‐Sidani, E., Merzenich, M. M., & Panizzutti, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064208 · Cited by 29
The importance of omega-3 fatty acids for behaviour, cognition and mood
Richardson, A. J. (2003) · Food & Nutrition Research · doi:10.3402/fnr.v47i2.1476 · Cited by 27
Aging and immune response to exercise
Shinkai, S., Konishi, M., & Shephard, R. J. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y98-043 · Cited by 27
Evaluation of objects and food for environmental enrichment of NZW rabbits.
Harris, L. D., Custer, L. B., Soranaka, E. T., et al. (2001) · PubMed · Cited by 22
Immune responses to inflammation and trauma: a physical training model
Shephard, R. J., & Shek, P. N. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y98-048 · Cited by 22
Mirrors as potential environmental enrichment for individually housed laboratory mice
Sherwin, C. M. (2004) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2003.12.014 · Cited by 21
Cellular responses to moderate and heavy exercise
Nehlsen‐Cannarella, S. L. (1998) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y98-050 · Cited by 20
Banks, W. A. (2008) · Springer eBooks · doi:10.1007/978-0-387-72573-4_4 · Cited by 16
Rašin, M. R., Darmopil, S., Petanjek, Z., Mahečić, T. T., Mohammed, A. H. S., & Bogdanović, N. (2011) · PubMed · Cited by 14
Zhang, H., Cai, R., Zhang, J., et al. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.07.054 · Cited by 14
Dinse, H. R. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00213.2004 · Cited by 11
Novel food items as environmental enrichment for rodents and rabbits
Brown, C. (2009) · Lab Animal · doi:10.1038/laban0409-119 · Cited by 10
Inflammation and neurodegeneration
Piehl, F. (2005) · Future Neurology · doi:10.2217/14796708.1.1.97 · Cited by 7
Jones, G. (2007) · Emergency Nurse · doi:10.7748/en.15.1.6.s10 · Cited by 5
The olfactory bulbectomized rat
Eisenstein, S. A. (2008) · Cited by 3
Metabolic syndrome and cognitive performance in the elderly
Rinaldi, M., Graffi, G., Gallone, S., & Rabino‐Massa, E. (2014) · Journal of Biological Research - Bollettino della Società Italiana di Biologia Sperimentale · doi:10.4081/jbr.2014.2132 · Cited by 1
Nilsson (1999) · doi:10.1002/(sici)1097-4695(19990615)39:4
Flagged first, then by citations
Research works printed but not linked: 3
- Fuglestad, 2008, “The role of nutrition in cognitive development,†in, Handbook in Developmental Cognitive Neuroscience, 623
- Haller, 2000, Anxiolytic effects of repeated victory in male Wistar rats., Aggressive Behavior, 26, 257, 10.1002/(SICI)1098-2337(2000)26:3257::AID-AB53.0.CO;2-7 · DOI
- Koletzko, 2003, Exercise and C-reactive protein., HEALTHY WEIGHT, 17
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
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
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
Regulation of astrocyte metabolism by mitochondrial translocator protein 18 kDa
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
Metadata
- 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
- 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
