Environmental enrichment attenuates hippocampal neuroinflammation and improves cognitive function during influenza infection

Brain, Behavior, and Immunity

Volumn 26, Issue 6, 2012, Pages 1006-1016

  Jurgens, Heidi A ^a   Johnson, Rodney W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

CD200; Cognition; Cytokines; Fractalkine; Hippocampus; Influenza; Microglia; Neuroinflammation; Neurotrophins

Indexed keywords

ALPHA INTERFERON; BRAIN DERIVED NEUROTROPHIC FACTOR; CD200 ANTIGEN; FRACTALKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; NERVE GROWTH FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENVIRONMENTAL ENRICHMENT; EXPOSURE; HIPPOCAMPUS; IMMUNOMODULATION; INFLUENZA; INFLUENZA VIRUS A H1N1; MALE; MAZE TEST; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; BODY WEIGHT; COGNITION; CYTOKINES; ENVIRONMENT; HIPPOCAMPUS; HOUSING, ANIMAL; IMMUNOLOGIC FACTORS; INFLAMMATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; MALE; MAZE LEARNING; MICE; MICE, INBRED BALB C; NERVE GROWTH FACTORS; ORTHOMYXOVIRIDAE INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84863862485     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.05.015     Document Type: Article

References (97)

1. Artola A., von Frijtag J.C., Fermont P.C.J., Gispen W.H., Schrama L.H., Kamal A., Spruijt B.M. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci. 2006, 23:261-272.
2. Bachstetter A.D., Morganti J.M., Jernberg J., Schlunk A., Mitchell S.H., Brewster K.W., Hudson C.E., Cole M.J., Harrison J.K., Bickford P.C., Gemma C. Fractalkine and CX 3 CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol. Aging 2011, 32:2030-2044.
3. Barrientos R.M., Sprunger D.B., Campeau S., Watkins L.R., Rudy J.W., Maier S.F. BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration. J. Neuroimmunol. 2004, 155:119-126.
4. Benaroya-Milshtein N., Hollander N., Apter A., Kukulansky T., Raz N., Wilf A., Yaniv I., Pick C.G. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. The European journal of neuroscience 2004, 20:1341-1347.
5. Bennett E.L., Rosenzwe M., Diamond M.C. Rat brain - effects of environmental enrichment on wet and dry weights. Science 1969, 163:825-874.
6. Beyer S., Raether G., Stadler K., Hoffrogge R., Scharf C., Rolfs A., Mix E., Strauss U. Interferon-beta modulates protein synthesis in the central nervous system. J. Neuroimmunol. 2009, 213:31-38.
7. Bovolenta R., Zucchini S., Paradiso B., Rodi D., Merigo F., Navarro Mora G., Osculati F., Berto E., Marconi P., Marzola A., Fabene P.F., Simonato M. Hippocampal FGF-2 and BDNF overexpression attenuates epileptogenesis-associated neuroinflammation and reduces spontaneous recurrent seizures. J. Neuroinflamm. 2010, 7:81.
8. Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci. 2005, 21:513-521.
9. Cardona A.E., Pioro E.P., Sasse M.E., Kostenko V., Cardona S.M., Dijkstra I.M., Huang D., Kidd G., Dombrowski S., Dutta R., Lee J.C., Cook D.N., Jung S., Lira S.A., Littman D.R., Ransohoff R.M. Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 2006, 9:917-924.
10. CDC Neurologic complications associated with novel influenza A (H1N1) virus infection in children - Dallas, Texas, May 2009. MMWR Morb. Mortal. Wkly Rep. 2009, 58:773-778.
11. Chitnis T., Imitola J., Wang Y., Elyaman W., Chawla P., Sharuk M., Raddassi K., Bronson R.T., Khoury S.J. Elevated neuronal expression of CD200 protects Wlds mice from inflammation-mediated neurodegeneration. Am. J. Pathol. 2007, 170:1695-1712.
12. Contet C., Rawlins J.N., Bannerman D.M. Faster is not surer-a comparison of C57BL/6J and 129S2/Sv mouse strains in the watermaze. Behav. Brain Res. 2001, 125:261-267.
13. Costello D.A., Lyons A., Browne T., Denieffe S., Cox F.F., Lynch M.A. Long-term potentiation is impaired in CD200-deficient mice. a role for Toll-like receptor activation 2011, The Journal of biological chemistry.
14. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 2007, 30:464-472.
15. Culley F.J. Natural killer cells in infection and inflammation of the lung. Immunology 2009, 128:151-163.
16. Cunningham C., Sanderson D.J. Malaise in the water maze: untangling the effects of LPS and IL-1beta on learning and memory. Brain Behav. Immun. 2008, 22:1117-1127.
17. de Sousa A.A., Reis R., Bento-Torres J., Trevia N., Lins N.A., Passos A., Santos Z., Diniz J.A., Vasconcelos P.F., Cunningham C., Perry V.H., Diniz C.W. Influence of enriched environment on viral encephalitis outcomes: behavioral and neuropathological changes in albino Swiss mice. PLoS ONE 2011, 6:e15597.
18. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 2001, 36:60-90.
19. Diamond M.C., Ingham C.A., Johnson R.E., Bennett E.L., Rosenzweig M.R. Effects of environment on morphology of rat cerebral-cortex and hippocampus. J. Neurobiol. 1976, 7:75-85.
20. Dong S., Li C., Wu P., Tsien J.Z., Hu Y. Environment enrichment rescues the neurodegenerative phenotypes in presenilins-deficient mice. Eur. J. Neurosci. 2007, 26:101-112.
21. Faherty C.J., Kerley D., Smeyne R.J. A golgi-cox morphological analysis of neuronal changes induced by environmental enrichment. Brain Res. Dev. Brain Res. 2003, 141:55-61.
22. Fox C., Merali Z., Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav. Brain Res. 2006, 175:1-8.
23. Goshen I., Kreisel T., Ounallah-Saad H., Renbaum P., Zalzstein Y., Ben-Hur T., Levy-Lahad E., Yirmiya R. A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 2007, 32:1106-1115.
24. Green E.J., Greenough W.T. Altered synaptic transmission in dentate gyrus of rats reared in complex environments - evidence from hippocampal slices maintained invitro. J. Neurophysiol. 1986, 55:739-750.
25. Green E.J., Greenough W.T., Schlumpf B.E. Effects of complex or isolated environments on cortical dendrites of middle-aged rats. Brain Res. 1983, 264:233-240.
26. Greenough W.T., Mcdonald J.W., Parnisari R.M., Camel J.E. Environmental-conditions modulate degeneration and new dendrite growth in cerebellum of senescent rats. Brain Res. 1986, 380:136-143.
27. Harrison J.K., Jiang Y., Chen S., Xia Y., Maciejewski D., McNamara R.K., Streit W.J., Salafranca M.N., Adhikari S., Thompson D.A., Botti P., Bacon K.B., Feng L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. USA 1998, 95:10896-10901.
28. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 1988, 12:123-137.
29. Hein A.M., Stasko M.R., Matousek S.B., Scott-McKean J.J., Maier S.F., Olschowka J.A., Costa A.C., O'Banion M.K. Sustained hippocampal IL-1beta overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav. Immun. 2010, 24:243-253.
30. Hoek R.M., Ruuls S.R., Murphy C.A., Wright G.J., Goddard R., Zurawski S.M., Blom B., Homola M.E., Streit W.J., Brown M.H., Barclay A.N., Sedgwick J.D. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 2000, 290:1768-1771.
31. Ickes B.R., Pham T.M., Sanders L.A., Albeck D.S., Mohammed A.H., Granholm A.C. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol. 2000, 164:45-52.
32. Juraska J.M., Kopcik J.R. Sex and environmental-influences on the size and ultrastructure of the rat corpus-callosum. Brain Res. 1988, 450:1-8.
33. Jurgens H.A., Amancherla K., Johnson R.W. Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J. Neurosci. 2012, 32:3958-3968.
34. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
35. Kesner R.P., Churchwell J.C. An analysis of rat prefrontal cortex in mediating executive function 2011, Neurobiol. Learn. Mem.
36. Kim T.S., Sun J., Braciale T.J. T cell responses during influenza infection: getting and keeping control. Trends Immunol. 2011, 32:225-231.
37. Kobilo T., Liu Q.R., Gandhi K., Mughal M., Shaham Y., van Praag H. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn. Mem. 2011, 18:605-609.
38. Konsman J.P., Parnet P., Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 2002, 25:154-159.
39. Larsson F., Winblad B., Mohammed A.H. Psychological stress and environmental adaptation in enriched vs. impoverished housed rats. Pharmacol. Biochem. Behav. 2002, 73:193-207.
40. Laviola G., Hannan A.J., Macri S., Solinas M., Jaber M. Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol. Dis. 2008, 31:159-168.
41. Leggio M.G., Mandolesi L., Federico F., Spirito F., Ricci B., Gelfo F., Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 2005, 163:78-90.
42. Lowder T., Padgett D.A., Woods J.A. Moderate exercise protects mice from death due to influenza virus. Brain Behav. Immun. 2005, 19:377-380.
43. Lowder T., Padgett D.A., Woods J.A. Moderate exercise early after influenza virus infection reduces the Th1 inflammatory response in lungs of mice. Exerc. Immunol. Rev. 2006, 12:97-111.
44. Lu Z.W., Hayley S., Ravindran A.V., Merali Z., Anisman H. Influence of psychosocial, psychogenic and neurogenic stressors on several aspects of immune functioning in mice. Stress 1999, 3:55-70.
45. Lynch M.A. Interleukin-1 beta exerts a myriad of effects in the brain and in particular in the hippocampus: analysis of some of these actions. Vitam. Horm. 2002, 64:185-219.
46. Lyons A., Lynch A.M., Downer E.J., Hanley R., O'Sullivan J.B., Smith A., Lynch M.A. Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attentuates microglial activation in vivo and in vitro. J. Neurochem. 2009, 110:1547-1556.
47. Maggi L., Scianni M., Branchi I., D'Andrea I., Lauro C., Limatola C. CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment. Front Cell Neurosci. 2011, 5:22.
48. Majde J.A. Neuroinflammation resulting from covert brain invasion by common viruses - a potential role in local and global neurodegeneration. Med. Hypotheses 2010, 75:204-213.
49. Marashi V., Barnekow A., Sachser N. Effects of environmental enrichment on males of a docile inbred strain of mice. Physiol. Behav. 2004, 82:765-776.
50. Markham J.A., Greenough W.T. Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol. 2004, 1:351-363.
51. Matsuoka, Y., Lamirande, E.W., Subbarao, K., 2009. The mouse model for influenza. Curr. Protoc. Microbiol. Chapter 15, Unit 15G 13.
52. McAfoose J., Baune B.T. Evidence for a cytokine model of cognitive function. Neurosci. Biobehav. Rev. 2009, 33:355-366.
53. McCoy M.K., Tansey M.G. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflamm. 2008, 5:45.
54. Mendoza-Fernandez V., Andrew R.D., Barajas-Lopez C. Interferon-alpha inhibits long-term potentiation and unmasks a long-term depression in the rat hippocampus. Brain Res. 2000, 885:14-24.
55. Mora F., Segovia G., del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res. Rev. 2007, 55:78-88.
56. Morris R.G. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 1984, 11:47-60.
57. Nilsson M., Perfilieva E., Johansson U., Orwar O., Eriksson P.S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 1999, 39:569-578.
58. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 2006, 7:697-709.
59. Nithianantharajah J., Levis H., Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol. Learn. Mem. 2004, 81:200-210.
60. Ojo, B., Rezaie, P., Gabbott, P.L., Davies, H., Colyer, F., Cowley, T.R., Lynch, M., Stewart, M.G., 2011. Age-related changes in the hippocampus (loss of synaptophysin and glial-synaptic interaction) are modified by systemic treatment with an NCAM-derived peptide, FGL. Brain Behav. Immun. 2012 Jul;26(5):778-88. Epub 2011 Oct 2.
61. Packer N., Pervaiz N., Hoffman-Goetz L. Does exercise protect from cognitive decline by altering brain cytokine and apoptotic protein levels? A systematic review of the literature. Exerc. Immunol. Rev. 2010, 16:138-162.
62. Paolicelli R.C., Bolasco G., Pagani F., Maggi L., Scianni M., Panzanelli P., Giustetto M., Ferreira T.A., Guiducci E., Dumas L., Ragozzino D., Gross C.T. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333:1456-1458.
63. Petrosini L., De Bartolo P., Foti F., Gelfo F., Cutuli D., Leggio M.G., Mandolesi L. On whether the environmental enrichment may provide cognitive and brain reserves. Brain Res. Rev. 2009, 61:221-239.
64. Pham T.M., Ickes B., Albeck D., Soderstrom S., Granholm A.C., Mohammed A.H. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 1999, 94:279-286.
65. Pickering M., O'Connor J.J. Pro-inflammatory cytokines and their effects in the dentate gyrus. Prog. Brain Res. 2007, 163:339-354.
66. Rampon C., Jiang C.H., Dong H., Tang Y.P., Lockhart D.J., Schultz P.G., Tsien J.Z., Hu Y.H. Effects of environmental enrichment on gene expression in the brain. P Natl Acad Sci USA 2000, 97:12880-12884.
67. Ransohoff R.M., Stevens B. Neuroscience. How many cell types does it take to wire a brain?. Science 2011, 333:1391-1392.
68. Ravenholt R.T., Foege W.H. 1918 influenza, encephalitis lethargica, parkinsonism. Lancet 1982, 2:860-864.
69. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 1996, 78:57-65.
70. Rossi C., Angelucci A., Costantin L., Braschi C., Mazzantini M., Babbini F., Fabbri M.E., Tessarollo L., Maffei L., Berardi N., Caleo M. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 2006, 24:1850-1856.
71. Sas A.R., Bimonte-Nelson H., Smothers C.T., Woodward J., Tyor W.R. Interferon-alpha causes neuronal dysfunction in encephalitis. J. Neurosci. 2009, 29:3948-3955.
72. Schlesinger R.W., Husak P.J., Bradshaw G.L., Panayotov P.P. Mechanisms involved in natural and experimental neuropathogenicity of influenza viruses: evidence and speculation. Adv. Virus Res. 1998, 50:289-379.
73. Schloesser R.J., Lehmann M., Martinowich K., Manji H.K., Herkenham M. Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Molecular psychiatry 2010, 15:1152-1163.
74. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
75. Simpson J., Kelly J.P. The impact of environmental enrichment in laboratory rats-behavioural and neurochemical aspects. Behav. Brain Res. 2011, 222:246-264.
76. Soffie M., Hahn K., Terao E., Eclancher F. Behavioural and glial changes in old rats following environmental enrichment. Behav. Brain Res. 1999, 101:37-49.
77. Sozda C.N., Hoffman A.N., Olsen A.S., Cheng J.P., Zafonte R.D., Kline A.E. Empirical comparison of typical and atypical environmental enrichment paradigms on functional and histological outcome after experimental traumatic brain injury. J. Neurotrauma 2010, 27:1047-1057.
78. Sparkman N.L., Buchanan J.B., Heyen J.R., Chen J., Beverly J.L., Johnson R.W. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J. Neurosci. 2006, 26:10709-10716.
79. Studahl M. Influenza virus and CNS manifestations. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology 2003, 28:225-232.
80. Tauber S.C., Bunkowski S., Ebert S., Schulz D., Kellert B., Nau R., Gerber J. Enriched environment fails to increase meningitis-induced neurogenesis and spatial memory in a mouse model of pneumococcal meningitis. J. Neurosci. Res. 2009, 87:1877-1883.
81. Tong L., Balazs R., Soiampornkul R., Thangnipon W., Cotman C.W. Interleukin-1 beta impairs brain derived neurotrophic factor-induced signal transduction. Neurobiol. Aging 2008, 29:1380-1393.
82. Tyler W.J., Alonso M., Bramham C.R., Pozzo-Miller L.D. From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem 2002, 9:224-237.
83. Van Dam D., Lenders G., De Deyn P.P. Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol. Learn. Mem. 2006, 85:164-172.
84. van Praag H. Exercise and the brain: something to chew on. Trends Neurosci. 2009, 32:283-290.
85. van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 2000, 1:191-198.
86. Viola G.G., Rodrigues L., Americo J.C., Hansel G., Vargas R.S., Biasibetti R., Swarowsky A., Goncalves C.A., Xavier L.L., Achaval M., Souza D.O., Amaral O.B. Morphological changes in hippocampal astrocytes induced by environmental enrichment in mice. Brain Res. 2009, 1274:47-54.
87. Voikar V., Polus A., Vasar E., Rauvala H. Long-term individual housing in C57BL/6J and DBA/2 mice. assessment of behavioral consequences. Genes, brain, and behavior 2005, 4:240-252.
88. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 2006, 1:848-858.
89. Walsh N.P., Gleeson M., Shephard R.J., Woods J.A., Bishop N.C., Fleshner M., Green C., Pedersen B.K., Hoffman-Goetz L., Rogers C.J., Northoff H., Abbasi A., Simon P. Position statement. Part one: Immune function and exercise. Exercise immunology review 2011, 17:6-63.
90. Wang G.F., Li W., Li K. Acute encephalopathy and encephalitis caused by influenza virus infection. Curr. Opin. Neurol. 2010, 23:305-311.
91. Waterhouse E.G., Xu B. New insights into the role of brain-derived neurotrophic factor in synaptic plasticity. Mol. Cell. Neurosci. 2009, 42:81-89.
92. Whishaw I.Q., Tomie J. Perseveration on place reversals in spatial swimming pool tasks: further evidence for place learning in hippocampal rats. Hippocampus 1997, 7:361-370.
93. Will B., Galani R., Kelche C., Rosenzweig M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog. Neurobiol. 2004, 72:167-182.
94. Williamson L.L., Chao A., Bilbo S.D. Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus. Brain Behav. Immun. 2012, 26:500-510.
95. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun. 2011, 25:181-213.
96. Ziv Y., Ron N., Butovsky O., Landa G., Sudai E., Greenberg N., Cohen H., Kipnis J., Schwartz M. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 2006, 9:268-275.
97. Zujovic V., Schussler N., Jourdain D., Duverger D., Taupin V. In vivo neutralization of endogenous brain fractalkine increases hippocampal TNFalpha and 8-isoprostane production induced by intracerebroventricular injection of LPS. J. Neuroimmunol. 2001, 115:135-143.