Environmental Enrichment and Gut Inflammation Modify Stress-Induced c-Fos Expression in the Mouse Corticolimbic System

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Reichmann, Florian ^a   Painsipp, Evelin ^a   Holzer, Peter ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; IODOACETAMIDE; MYELOPEROXIDASE; PROTEIN C FOS;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN DEPTH STIMULATION; COLITIS; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ACTIVITY SCORE; DISEASE EXACERBATION; ENVIRONMENTAL ENRICHMENT; EVOKED RESPONSE; GASTRITIS; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; LIMBIC CORTEX; MALE; MENTAL STRESS; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; STRESS MANAGEMENT; WATER STRESS;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CEREBRAL CORTEX; COLITIS; DEXTRAN SULFATE; GASTRITIS; GENE EXPRESSION; INFLAMMATION; IODOACETAMIDE; MALE; MICE; NEURONAL PLASTICITY; PROTO-ONCOGENE PROTEINS C-FOS; STRESS, PHYSIOLOGICAL;

MUS; RODENTIA;

EID: 84872564643     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054811     Document Type: Article

References (101)

1. van Praag H, Kempermann G, Gage FH, (2000) Neural consequences of environmental enrichment. Nature Reviews. Neuroscience 1: 191-198.
2. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, et al. (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behavioural Brain Research 163: 78-90.
3. Meshi D, Drew MR, Saxe M, Ansorge MS, David D, et al. (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nature Neuroscience 9: 729-731.
4. Roy V, Belzung C, Delarue C, Chapillon P, (2001) Environmental enrichment in BALB/c mice: Effects in classical tests of anxiety and exposure to a predatory odor. Physiology & Behavior 74: 313-320.
5. Van de Weerd HA, Aarsen EL, Mulder A, Kruitwagen CL, Hendriksen CF, et al. (2002) Effects of environmental enrichment for mice: Variation in experimental results. Journal of Applied Animal Welfare Science: JAAWS 5: 87-109.
6. Van Loo PL, Van der Meer E, Kruitwagen CL, Koolhaas JM, Van Zutphen LF, et al. (2004) Long-term effects of husbandry procedures on stress-related parameters in male mice of two strains. Laboratory Animals 38: 169-177.
7. Green TA, Alibhai IN, Roybal CN, Winstanley CA, Theobald DE, et al. (2010) Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biological Psychiatry 67: 28-35.
8. Sztainberg Y, Kuperman Y, Tsoory M, Lebow M, Chen A, (2010) The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1. Molecular Psychiatry 15: 905-917.
9. Lin EJ, Choi E, Liu X, Martin A, During MJ, (2011) Environmental enrichment exerts sex-specific effects on emotionality in C57BL/6J mice. Behavioural Brain Research 216: 349-357.
10. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, et al. (2000) Effects of environmental enrichment on gene expression in the brain. Proceedings of the National Academy of Sciences of the United States of America 97: 12880-12884.
11. Rizzi S, Bianchi P, Guidi S, Ciani E, Bartesaghi R, (2011) Impact of environmental enrichment on neurogenesis in the dentate gyrus during the early postnatal period. Brain Research 1415: 23-33.
12. Kempermann G, Kuhn HG, Gage FH, (1998) Experience-induced neurogenesis in the senescent dentate gyrus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 18: 3206-3212.
13. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, et al. (2000) Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Experimental Neurology 164: 45-52.
14. Pham TM, Ickes B, Albeck D, Soderstrom S, Granholm AC, et al. (1999) Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94: 279-286.
15. Zhu SW, Yee BK, Nyffeler M, Winblad B, Feldon J, et al. (2006) Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behavioural Brain Research 169: 10-20.
16. Brenes JC, Padilla M, Fornaguera J, (2009) A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behavioural Brain Research 197: 125-137.
17. Belz EE, Kennell JS, Czambel RK, Rubin RT, Rhodes ME, (2003) Environmental enrichment lowers stress-responsive hormones in singly housed male and female rats. Pharmacology, Biochemistry, and Behavior 76: 481-486.
18. Morley-Fletcher S, Rea M, Maccari S, Laviola G, (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. The European Journal of Neuroscience 18: 3367-3374.
19. Schloesser RJ, Lehmann M, Martinowich K, Manji HK, Herkenham M, (2010) Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Molecular Psychiatry 15: 1152-1163.
20. Schrijver NC, Bahr NI, Weiss IC, Wurbel H, (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacology, Biochemistry, and Behavior 73: 209-224.
21. Tall JM, (2009) Housing supplementation decreases the magnitude of inflammation-induced nociception in rats. Behavioural Brain Research 197: 230-233.
22. Gabriel AF, Paoletti G, Della Seta D, Panelli R, Marcus MA, et al. (2010) Enriched environment and the recovery from inflammatory pain: Social versus physical aspects and their interaction. Behavioural Brain Research 208: 90-95.
23. Shum FW, Wu LJ, Zhao MG, Toyoda H, Xu H, et al. (2007) Alteration of cingulate long-term plasticity and behavioral sensitization to inflammation by environmental enrichment. Learning & Memory (Cold Spring Harbor, N.Y.) 14: 304-312.
24. Kovacs KJ, (1998) c-fos as a transcription factor: A stressful (re)view from a functional map. Neurochemistry International 33: 287-297.
25. Bradesi S, Schwetz I, Ennes HS, Lamy CM, Ohning G, et al. (2005) Repeated exposure to water avoidance stress in rats: A new model for sustained visceral hyperalgesia. American Journal of Physiology. Gastrointestinal and Liver Physiology 289: G42-53.
26. Lamb K, Kang YM, Gebhart GF, Bielefeldt K, (2003) Gastric inflammation triggers hypersensitivity to acid in awake rats. Gastroenterology 125: 1410-1418.
27. Wultsch T, Painsipp E, Shahbazian A, Mitrovic M, Edelsbrunner M, et al. (2008) Deletion of the acid-sensing ion channel ASIC3 prevents gastritis-induced acid hyperresponsiveness of the stomach-brainstem axis. Pain 134: 245-253.
28. Eijkelkamp N, Kavelaars A, Elsenbruch S, Schedlowski M, Holtmann G, et al. (2007) Increased visceral sensitivity to capsaicin after DSS-induced colitis in mice: Spinal cord c-fos expression and behavior. American Journal of Physiology. Gastrointestinal and Liver Physiology 293: G749-57.
29. Mitrovic M, Shahbazian A, Bock E, Pabst MA, Holzer P, (2010) Chemo-nociceptive signalling from the colon is enhanced by mild colitis and blocked by inhibition of transient receptor potential ankyrin 1 channels. British Journal of Pharmacology 160: 1430-1442.
30. Kresse AE, Million M, Saperas E, Tache Y, (2001) Colitis induces CRF expression in hypothalamic magnocellular neurons and blunts CRF gene response to stress in rats. American Journal of Physiology. Gastrointestinal and Liver Physiology 281: G1203-13.
31. Cakir B, Bozkurt A, Ercan F, Yegen BC, (2004) The anti-inflammatory effect of leptin on experimental colitis: Involvement of endogenous glucocorticoids. Peptides 25: 95-104.
32. Melgar S, Engstrom K, Jagervall A, Martinez V, (2008) Psychological stress reactivates dextran sulfate sodium-induced chronic colitis in mice. Stress (Amsterdam, Netherlands) 11: 348-362.
33. Larsson MH, Miketa A, Martinez V, (2009) Lack of interaction between psychological stress and DSS-induced colitis affecting colonic sensitivity during colorectal distension in mice. Stress (Amsterdam, Netherlands) 12: 434-444.
34. Cetinel S, Hancioglu S, Sener E, Uner C, Kilic M, et al. (2010) Oxytocin treatment alleviates stress-aggravated colitis by a receptor-dependent mechanism. Regulatory Peptides 160: 146-152.
35. Ibeakanma C, Ochoa-Cortes F, Miranda-Morales M, McDonald T, Spreadbury I, et al. (2011) Brain-gut interactions increase peripheral nociceptive signaling in mice with postinfectious irritable bowel syndrome. Gastroenterology 141: 2098-2108.e5.
36. Tache Y, Perdue MH, (2004) Role of peripheral CRF signalling pathways in stress-related alterations of gut motility and mucosal function. Neurogastroenterology and Motility: The Official Journal of the European Gastrointestinal Motility Society 16Suppl 1: 137-142.
37. Velin AK, Ericson AC, Braaf Y, Wallon C, Soderholm JD, (2004) Increased antigen and bacterial uptake in follicle associated epithelium induced by chronic psychological stress in rats. Gut 53: 494-500.
38. Mawdsley JE, Rampton DS, (2005) Psychological stress in IBD: New insights into pathogenic and therapeutic implications. Gut 54: 1481-1491.
39. Chang L, (2011) The role of stress on physiologic responses and clinical symptoms in irritable bowel syndrome. Gastroenterology 140: 761-765.
40. Mayer EA, (2011) Gut feelings: The emerging biology of gut-brain communication. Nature Reviews. Neuroscience 12: 453-466.
41. Marashi V, Barnekow A, Ossendorf E, Sachser N, (2003) Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Hormones and Behavior 43: 281-292.
42. Van de Weerd HA, Van Loo PL, Van Zutphen LF, Koolhaas JM, Baumans V, (1997) Preferences for nesting material as environmental enrichment for laboratory mice. Laboratory Animals 31: 133-143.
43. Sherwin CM, (1997) Observations on the prevalence of nest-building in non-breeding TO strain mice and their use of two nesting materials. Laboratory Animals 31: 125-132.
44. Jennings M, Batchelor GR, Brain PF, Dick A, Elliott H, et al. (1998) Refining rodent husbandry: The mouse. report of the rodent refinement working party. Laboratory Animals 32: 233-259.
45. Painsipp E, Wultsch T, Shahbazian A, Edelsbrunner M, Kreissl MC, et al. (2007) Experimental gastritis in mice enhances anxiety in a gender-related manner. Neuroscience 150: 522-536.
46. Davis S, Butcher SP, Morris RG, (1992) The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 12: 21-34.
47. Holscher C, (1999) Stress impairs performance in spatial water maze learning tasks. Behavioural Brain Research 100: 225-235.
48. Limback-Stokin K, Korzus E, Nagaoka-Yasuda R, Mayford M, (2004) Nuclear calcium/calmodulin regulates memory consolidation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 24: 10858-10867.
49. Krawisz JE, Sharon P, Stenson WF, (1984) Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. assessment of inflammation in rat and hamster models. Gastroenterology 87: 1344-1350.
50. Sundquist SJ, Nisenbaum LK, (2005) Fast fos: Rapid protocols for single- and double-labeling c-fos immunohistochemistry in fresh frozen brain sections. Journal of Neuroscience Methods 141: 9-20.
51. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. San Diego, California: Academic Press.
52. Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design. New York: McGraw-Hill.
53. Kirk RE (1995) Experimental design: Procedures for the behavioral sciences. Pacific Grove, California: Brooks/Cole.
54. Hays WL (2007) Statistics. Belmont: Wadsworth.
55. Wurbel H, (2001) Ideal homes? housing effects on rodent brain and behaviour. Trends in Neurosciences 24: 207-211.
56. Painsipp E, Herzog H, Sperk G, Holzer P, (2011) Sex-dependent control of murine emotional-affective behaviour in health and colitis by peptide YY and neuropeptide Y. British Journal of Pharmacology. 163: 1302-1314.
57. Amaral OB, Vargas RS, Hansel G, Izquierdo I, Souza DO, (2008) Duration of environmental enrichment influences the magnitude and persistence of its behavioral effects on mice. Physiology & Behavior 93: 388-394.
58. Senba E, Ueyama T, (1997) Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neuroscience Research 29: 183-207.
59. Lopez JF, Akil H, Watson SJ, (1999) Neural circuits mediating stress. Biological Psychiatry 46: 1461-1471.
60. Martinez M, Calvo-Torrent A, Herbert J, (2002) Mapping brain response to social stress in rodents with c-fos expression: A review. Stress (Amsterdam, Netherlands) 5: 3-13.
61. Bonaz B, Tache Y, (1994) Water-avoidance stress-induced c-fos expression in the rat brain and stimulation of fecal output: Role of corticotropin-releasing factor. Brain Research 641: 21-28.
62. O'Mahony CM, Sweeney FF, Daly E, Dinan TG, Cryan JF, (2010) Restraint stress-induced brain activation patterns in two strains of mice differing in their anxiety behaviour. Behavioural Brain Research 213: 148-154.
63. Luckman SM, Dyball RE, Leng G, (1994) Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 14: 4825-4830.
64. Kovacs KJ, (2008) Measurement of immediate-early gene activation- c-fos and beyond. Journal of Neuroendocrinology 20: 665-672.
65. Hendriksen H, Prins J, Olivier B, Oosting RS, (2010) Environmental enrichment induces behavioral recovery and enhanced hippocampal cell proliferation in an antidepressant-resistant animal model for PTSD. PloS One 5: e11943.
66. Llorens-Martin MV, Rueda N, Martinez-Cue C, Torres-Aleman I, Florez J, et al. (2007) Both increases in immature dentate neuron number and decreases of immobility time in the forced swim test occurred in parallel after environmental enrichment of mice. Neuroscience 147: 631-638.
67. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, et al. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. The European Journal of Neuroscience 17: 2042-2046.
68. Altman J, Das GD, (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. The Journal of Comparative Neurology 124: 319-335.
69. Kempermann G, Kuhn HG, Gage FH, (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495.
70. Mora F, Segovia G, del Arco A, (2007) Aging, plasticity and environmental enrichment: Structural changes and neurotransmitter dynamics in several areas of the brain. Brain Research Reviews 55: 78-88.
71. Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A, (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Annals of the New York Academy of Sciences 911: 369-391.
72. Ishikawa A, Nakamura S, (2003) Convergence and interaction of hippocampal and amygdalar projections within the prefrontal cortex in the rat. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 23: 9987-9995.
73. McEwen BS, (2007) Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews 87: 873-904.
74. Knapska E, Maren S, (2009) Reciprocal patterns of c-fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learning & Memory (Cold Spring Harbor, N.Y.) 16: 486-493.
75. Pinard CR, Mascagni F, McDonald AJ, (2012) Medial prefrontal cortical innervation of the intercalated nuclear region of the amygdala. Neuroscience 205: 112-124.
76. Roozendaal B, McEwen BS, Chattarji S, (2009) Stress, memory and the amygdala. Nature Reviews. Neuroscience 10: 423-433.
77. Ulrich-Lai YM, Herman JP, (2009) Neural regulation of endocrine and autonomic stress responses. Nature Reviews. Neuroscience 10: 397-409.
78. Amano T, Duvarci S, Popa D, Pare D, (2011) The fear circuit revisited: Contributions of the basal amygdala nuclei to conditioned fear. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 31: 15481-15489.
79. Spannuth BM, Hale MW, Evans AK, Lukkes JL, Campeau S, et al. (2011) Investigation of a central nucleus of the amygdala/dorsal raphe nucleus serotonergic circuit implicated in fear-potentiated startle. Neuroscience 179: 104-119.
80. Moncek F, Duncko R, Johansson BB, Jezova D, (2004) Effect of environmental enrichment on stress related systems in rats. Journal of Neuroendocrinology 16: 423-431.
81. Larsson F, Winblad B, Mohammed AH, (2002) Psychological stress and environmental adaptation in enriched vs. impoverished housed rats. Pharmacology, Biochemistry, and Behavior 73: 193-207.
82. Zimmermann A, Stauffacher M, Langhans W, Wurbel H, (2001) Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behavioural Brain Research 121: 11-20.
83. Segovia G, Del Arco A, de Blas M, Garrido P, Mora F, (2008) Effects of an enriched environment on the release of dopamine in the prefrontal cortex produced by stress and on working memory during aging in the awake rat. Behavioural Brain Research 187: 304-311.
84. Segovia G, Del Arco A, Garrido P, de Blas M, Mora F, (2008) Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging. Neurochemistry International 52: 1198-1203.
85. von Bohlen und Halbach O, Albrecht D, (2002) Reciprocal connections of the hippocampal area CA1, the lateral nucleus of the amygdala and cortical areas in a combined horizontal slice preparation. Neuroscience Research 44: 91-100.
86. Akirav I, Sandi C, Richter-Levin G, (2001) Differential activation of hippocampus and amygdala following spatial learning under stress. The European Journal of Neuroscience 14: 719-725.
87. Kim JJ, Lee HJ, Han JS, Packard MG, (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 21: 5222-5228.
88. Herman JP, Cullinan WE, (1997) Neurocircuitry of stress: Central control of the hypothalamo-pituitary-adrenocortical axis. Trends in Neurosciences 20: 78-84.
89. Benaroya-Milshtein N, Hollander N, Apter A, Kukulansky T, Raz N, et al. (2004) Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. The European Journal of Neuroscience 20: 1341-1347.
90. Fox C, Merali Z, Harrison C, (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behavioural Brain Research 175: 1-8.
91. de Sousa AA, Reis R, Bento-Torres J, Trevia N, Lins NA, et al. (2011) Influence of enriched environment on viral encephalitis outcomes: Behavioral and neuropathological changes in albino swiss mice. PloS One 6: e15597.
92. Snoek SA, Verstege MI, Boeckxstaens GE, van den Wijngaard RM, de Jonge WJ, (2010) The enteric nervous system as a regulator of intestinal epithelial barrier function in health and disease. Expert Review of Gastroenterology & Hepatology 4: 637-651.
93. Kitajima S, Takuma S, Morimoto M, (1999) Changes in colonic mucosal permeability in mouse colitis induced with dextran sulfate sodium. Experimental Animals/Japanese Association for Laboratory Animal Science 48: 137-143.
94. Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, et al. (2009) Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PloS One 4: e6073.
95. Johansson ME, Gustafsson JK, Sjoberg KE, Petersson J, Holm L, et al. (2010) Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PloS One 5: e12238.
96. Nagalingam NA, Kao JY, Young VB, (2011) Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis. Inflammatory Bowel Diseases 17: 917-926.
97. Iwaya H, Maeta K, Hara H, Ishizuka S, (2012) Mucosal permeability is an intrinsic factor in susceptibility to dextran sulfate sodium-induced colitis in rats. Experimental Biology and Medicine (Maywood, N.J.) 237: 451-460.
98. Elsenbruch S, Rosenberger C, Bingel U, Forsting M, Schedlowski M, et al. (2010) Patients with irritable bowel syndrome have altered emotional modulation of neural responses to visceral stimuli. Gastroenterology 139: 1310-1319.
99. Busnardo C, Tavares RF, Resstel LB, Elias LL, Correa FM, (2010) Paraventricular nucleus modulates autonomic and neuroendocrine responses to acute restraint stress in rats. Autonomic Neuroscience: Basic & Clinical 158: 51-57.
100. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, et al. (2011) Bacterial infection causes stress-induced memory dysfunction in mice. Gut 60: 307-317.
101. Harbuz MS, Rooney C, Jones M, Ingram CD, (1999) Hypothalamo-pituitary-adrenal axis responses to lipopolysaccharide in male and female rats with adjuvant-induced arthritis. Brain, Behavior, and Immunity 13: 335-347.