Enriched housing enhances recovery of limb placement ability and reduces aggrecan-containing perineuronal nets in the rat somatosensory cortex after experimental stroke

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Madinier, Alexandre ^a   Quattromani, Miriana Jlenia ^a   Sjölund, Carin ^a   Ruscher, Karsten ^a   Wieloch, Tadeusz ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; GLYCAN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; BRAIN INFARCTION SIZE; CELL COUNTING; CONTROLLED STUDY; ENRICHED HOUSING ENVIRONMENT; EXPERIMENTAL STROKE; FORELIMB; HINDLIMB; HOUSING; IMMUNOREACTIVITY; KINESTHESIA; MALE; MOTOR PERFORMANCE; NERVE SHEATH; NONHUMAN; PROPRIOCEPTION; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; RAT; SENSORIMOTOR FUNCTION; SOMATOSENSORY CORTEX; TACTILE DISCRIMINATION; TASK PERFORMANCE; VISION; ANIMAL; CEREBROVASCULAR ACCIDENT; METABOLISM; NERVE CELL NETWORK; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TOUCH;

AGGRECANS; ANIMALS; HINDLIMB; MALE; NERVE NET; PROPRIOCEPTION; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; STROKE; TOUCH PERCEPTION;

EID: 84899712735     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093121     Document Type: Article

References (91)

1. Roger VL, Go AS, Lloyd Jones DM, Benjamin EJ, Berry JD, et al. (2012) Heart disease and stroke statistics - 2012 update: a report from the American Heart Association. Circulation 125: e2-e220.
2. Jørgensen HS, Nakayama H, Raaschou HO, Vive Larsen J, Støier M, et al. (1995) Outcome and time course of recovery in stroke. Part I: Outcome. The Copenhagen Stroke Study. Arch Phys Med Rehabil 76: 399-405.
3. Carey LM, Oke LE, Matyas TA (1996) Impaired limb position sense after stroke: a quantitative test for clinical use. Arch Phys Med Rehabil 77: 1271-1278. (Pubitemid 26424841)
4. Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J (1992) Measurement of motor recovery after stroke. Outcome assessment and sample size requirements. Stroke 23: 1084-1089.
5. Muntner P, Garrett E, Klag MJ, Coresh J (2002) Trends in stroke prevalence between 1973 and 1991 in the US population 25 to 74 years of age. Stroke 33: 1209-1213. (Pubitemid 34517037)
6. Carey LM, Abbott DF, Harvey MR, Puce A, Seitz RJ, et al. (2011) Relationship between touch impairment and brain activation after lesions of subcortical and cortical somatosensory regions. Neurorehabil Neural Repair 25: 443-457.
7. Kitago T, Liang J, Huang VS, Hayes S, Simon P, et al. (2013) Improvement after constraint-induced movement therapy: recovery of normal motor control or task-specific compensation? Neurorehabil Neural Repair 27: 99-109.
8. Edwardson MA, Lucas TH, Carey JR, Fetz EE (2013) New modalities of brain stimulation for stroke rehabilitation. Exp Brain Res 224: 335-358.
9. Schulz R, Gerloff C, Hummel FC (2013) Non-invasive brain stimulation in neurological diseases. Neuropharmacology 64: 579-587.
10. Murphy TH, Corbett D (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 10: 861-872.
11. Dancause N (2006) Neurophysiological and anatomical plasticity in the adult sensorimotor cortex. Rev Neurosci 580: 561-580.
12. Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697-709. (Pubitemid 44267494)
13. Hebb DO (1947) The effects of early experience on problem solving at maturity. Am Psychol 2: 306-307.
14. Van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1: 191-198.
15. Hockly E, Cordery PM, Woodman B, Mahal A, van Dellen A, et al. (2002) Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Ann Neurol 51: 235-242. (Pubitemid 34111446)
16. Arendash GW, Garcia MF, Costa DA, Cracchiolo JR, Wefes IM, et al. (2004) Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. Neuroreport 15: 1751-1754. (Pubitemid 39062588)
17. Bezard E, Dovero S, Belin D, Duconger S, Jackson Lewis V, et al. (2003) Enriched environment confers resistance to 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J Neurosci 23: 10999-11007. (Pubitemid 37548933)
18. Restivo L, Ferrari F, Passino E, Sgobio C, Bock J, et al. (2005) Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc Natl Acad Sci U S A 102: 11557-11562. (Pubitemid 41153858)
19. Martínez Cué C, Rueda N, García E, Davisson MT, Schmidt C, et al. (2005) Behavioral, cognitive and biochemical responses to different environmental conditions in male Ts65Dn mice, a model of Down syndrome. Behav Brain Res 163: 174-185. (Pubitemid 41138051)
20. Kovesdi E, Gyorgy AB, Kwon SK, Wingo DL, Kamnaksh A, et al. (2011) The effect of enriched environment on the outcome of traumatic brain injury; a behavioral, proteomics, and histological study. Front Neurosci 5: 1-12.
21. Janssen H, Bernhardt J, Collier JM, Sena ES, McElduff P, et al. (2010) An enriched environment improves sensorimotor function post-ischemic stroke. Neurorehabil Neural Repair 24: 802-813.
22. Ohlsson AL, Johansson BB (1995) Environment influences functional outcome of cerebral infarction in rats. Stroke 26: 644-649.
23. Wieloch T, Nikolich K (2006) Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 16: 258-264. (Pubitemid 43949227)
24. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, et al. (2000) Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci 97: 12880-12884.
25. Keyvani K, Sachser N, Witte OW, Paulus W (2004) Gene expression profiling in the intact and injured brain following environmental enrichment. J Neuropathol Exp Neurol 63: 598-609. (Pubitemid 38736423)
26. Ruscher K, Johannesson E, Brugiere E, Erickson A, Rickhag M, et al. (2009) Enriched environment reduces apolipoprotein E (ApoE) in reactive astrocytes and attenuates inflammation of the peri-infarct tissue after experimental stroke. J Cereb Blood Flow Metab 29: 1796-1805.
27. Inácio AR, Ruscher K, Wieloch T (2011) Enriched environment downregulates macrophage migration inhibitory factor and increases parvalbumin in the brain following experimental stroke. Neurobiol Dis 41: 270-278.
28. Johansson BB, Belichenko PV (2002) Neuronal plasticity and dendritic spines: effect of environmental enrichment on intact and postischemic rat brain. J Cereb Blood Flow Metab 22: 89-96. (Pubitemid 34038387)
29. Biernaskie J, Corbett D (2001) Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 21: 5272-5280. (Pubitemid 32622952)
30. Frischknecht R, Gundelfinger ED (2012) The brain's extracellular matrix and its role in synaptic plasticity. Adv Exp Med Biol 970: 153-171.
31. Rosell A, Lo EH (2008) Multiphasic roles for matrix metalloproteinases after stroke. Curr Opin Pharmacol 8: 82-89.
32. Soleman S, Filippov MA, Dityatev A, Fawcett JW (2013) Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253: 194-213.
33. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4: 399-415. (Pubitemid 37280178)
34. Viapiano MS, Matthews RT (2006) From barriers to bridges: chondroitin sulfate proteoglycans in neuropathology. Trends Mol Med 12: 488-496. (Pubitemid 44441998)
35. Wang D, Fawcett J (2012) The perineuronal net and the control of CNS plasticity. Cell Tissue Res 349: 147-160.
36. Hockfield S, Mckay RD (1983) A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc Natl Acad Sci U S A 80: 5758-5761. (Pubitemid 14249907)
37. Celio MR, Spreafico R, De Biasi S, Vitellaro Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21: 510-515. (Pubitemid 28555691)
38. Morawski M, Brückner G, Arendt T, Matthews RT (2012) Aggrecan: beyond cartilage and into the brain. Int J Biochem Cell Biol 44: 690-693.
39. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80: 1267-1290.
40. Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57: 276-289.
41. Matthews RT, Kelly GM, Zerillo CA, Gray G, Tiemeyer M, et al. (2002) Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 22: 7536-7547. (Pubitemid 35386355)
42. Guimarães A, Zaremba S, Hockfield S (1990) Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J Neurosci 10: 3014-3024.
43. McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT (2007) Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 27: 5405-5413. (Pubitemid 46790165)
44. Härtig W, Brauer K, Bigl V, Brückner G (1994) Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labeled perineuronal nets around parvalbumin-containing neurons. Brain Res 635: 307-311.
45. Hockfield S, Kalb RG, Zaremba S, Fryer H (1990) Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb Symp Quant Biol 55: 505-514.
46. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, et al. (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298: 1248-1251. (Pubitemid 35285495)
47. Harris NG, Carmichael ST, Hovda DA, Sutton RL (2009) Traumatic brain injury results in disparate regions of chondroitin sulfate proteoglycan expression that are temporally limited. J Neurosci Res 87: 2937-2950.
48. Harris NG, Mironova YA, Hovda DA, Sutton RL (2010) Pericontusion axon sprouting is spatially and temporally consistent with a growth-permissive environment after traumatic brain injury. J Neuropathol Exp Neurol 69: 139-154.
49. Hobohm C, Günther A, Grosche J, Rossner S, Schneider D, et al. (2005) Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats. J Neurosci Res 80: 539-548. (Pubitemid 40780814)
50. Carmichael ST, Archibeque I, Luke L, Nolan T, Momiy J, et al. (2005) Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 193: 291-311. (Pubitemid 40616180)
51. Karetko Sysa M, Skangiel Kramska J, Nowicka D (2011) Disturbance of perineuronal nets in the perilesional area after photothrombosis is not associated with neuronal death. Exp Neurol 231: 113-126.
52. Ruscher K, Shamloo M, Rickhag M, Ladunga I, Soriano L, et al. (2011) The sigma-1 receptor enhances brain plasticity and functional recovery after experimental stroke. Brain 134: 732-746.
53. Encarnacion A, Horie N, Keren Gill H, Bliss TM, Steinberg GK, et al. (2011) Long-term behavioral assessment of function in an experimental model for ischemic stroke. J Neurosci Methods 196: 247-257.
54. Lenzlinger PM, Saatman KE, Hoover RC, Cheney JA, Bareyre FM, et al. (2004) Inhibition of vascular endothelial growth factor receptor (VEGFR) signaling by BSF476921 attenuates regional cerebral edema following traumatic brain injury in rats. Restor Neurol Neurosci 22: 73-79. (Pubitemid 38850335)
55. De Ryck M, Van Reempts J, Duytschaever H, Van Deuren B, Clincke G (1992) Neocortical localization of tactile/proprioceptive limb placing reactions in the rat. Brain Res 573: 44-60.
56. Hua Y, Schallert T, Keep RF, Wu J, Hoff JT, et al. (2002) Behavioral tests after intracerebral hemorrhage in the rat. Stroke 33: 2478-2484.
57. Jones TA, Schallert T (1992) Subcortical deterioration after cortical damage: effects of diazepam and relation to recovery of function. Behav Brain Res 51: 1-13.
58. Ballermann M, Metz GA, McKenna JE, Klassen F, Whishaw IQ (2001) The pasta matrix reaching task: a simple test for measuring skilled reaching distance, direction, and dexterity in rats. J Neurosci Methods 106: 39-45. (Pubitemid 32193013)
59. Swanson RA, Morton MT, Tsao Wu G, Savalos RA, Davidson C, et al. (1990) A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10: 290-293. (Pubitemid 20096202)
60. Giamanco KA, Morawski M, Matthews RT (2010) Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 170: 1314-1327.
61. Lendvai D, Morawski M, Négyessy L, Gáti G, Jäger C, et al. (2013) Neurochemical mapping of the human hippocampus reveals perisynaptic matrix around functional synapses in Alzheimer's disease. Acta Neuropathol 125: 215-229.
62. Dino MR, Harroch S, Hockfield S, Matthews RT (2006) Monoclonal antibody Cat-315 detects a glycoform of receptor protein tyrosine phosphatase beta/ phosphacan early in CNS development that localizes to extrasynaptic sites prior to synapse formation. Neuroscience 142: 1055-1069. (Pubitemid 44636060)
63. Sigler A, Goroshkov A, Murphy TH (2008) Hardware and methodology for targeting single brain arterioles for photothrombotic stroke on an upright microscope. J Neurosci Methods 170: 35-44.
64. Moon SK, Alaverdashvili M, Cross AR, Whishaw IQ (2009) Both compensation and recovery of skilled reaching following small photothrombotic stroke to motor cortex in the rat. Exp Neurol 218: 145-153.
65. Starkey ML, Bleul C, Zörner B, Lindau NT, Mueggler T, et al. (2012) Back seat driving: hindlimb corticospinal neurons assume forelimb control following ischaemic stroke. Brain 135: 3265-3281.
66. Diederich K, Quennet V, Bauer H, Müller HD, Wersching H, et al. (2012) Successful regeneration after experimental stroke by granulocyte-colony stimulating factor is not further enhanced by constraint-induced movement therapy either in concurrent or in sequential combination therapy. Stroke 43: 185-192.
67. Jin Z, Wu J, Oh SY, Kim KW, Shin BS (2010) The effect of stress on stroke recovery in a photothrombotic stroke animal model. Brain Res 1363: 191-197.
68. Minnerup J, Seeger FH, Kuhnert K, Diederich K, Schilling M, et al. (2010) Intracarotid administration of human bone marrow mononuclear cells in rat photothrombotic ischemia. Exp Transl Stroke Med 2: 3.
69. Jablonka JA, Burnat K, Witte OW, Kossut M (2010) Remapping of the somatosensory cortex after a photothrombotic stroke: dynamics of the compensatory reorganization. Neuroscience 165: 90-100.
70. Vandeputte C, Taymans JM, Casteels C, Coun F, Ni Y, et al. (2010) Automated quantitative gait analysis in animal models of movement disorders. BMC Neurosci 11: 92.
71. Knieling M, Metz GA, Antonow Schlorke I, Witte OW (2009) Enriched environment promotes efficiency of compensatory movements after cerebral ischemia in rats. Neuroscience 163: 759-769.
72. Müller HD, Hanumanthiah KM, Diederich K, Schwab S, Schäbitz WR, et al. (2008) Brain-derived neurotrophic factor but not forced arm use improves longterm outcome after photothrombotic stroke and transiently upregulates binding densities of excitatory glutamate receptors in the rat brain. Stroke 39: 1012-1021.
73. Rogers DC, Hunter AJ (1997) Photothrombotic lesions of the rat cortex impair acquisition of the water maze. Pharmacol Biochem Behav 56: 747-754. (Pubitemid 27189761)
74. Schäbitz WR, Berger C, Kollmar R, Seitz M, Tanay E, et al. (2004) Effect of brain-derived neurotrophic factor treatment and forced arm use on functional motor recovery after small cortical ischemia. Stroke 35: 992-997. (Pubitemid 38419816)
75. Wood NI, Sopesen BV, Roberts JC, Pambakian P, Rothaul AL, et al. (1996) Motor dysfunction in a photothrombotic focal ischaemia model. Behav Brain Res 78: 113-120. (Pubitemid 26252880)
76. Donoghue JP, Sanes JN (1994) Motor areas of the cerebral cortex. J Clin Neurophysiol 11: 382-396. (Pubitemid 24243023)
77. Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66: 23-38.
78. De Ryck M, Van Reempts J, Borgers M, Wauquier A, Janssen PA (1989) Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 20: 1383-1390. (Pubitemid 19254555)
79. Shanina EV, Schallert T, Witte OW, Redecker C (2006) Behavioral recovery from unilateral photothrombotic infarcts of the forelimb sensorimotor cortex in rats: role of the contralateral cortex. Neuroscience 139: 1495-1506.
80. Wang Y, Bontempi B, Hong SM, Mehta K, Weinstein PR, et al. (2008) A comprehensive analysis of gait impairment after experimental stroke and the therapeutic effect of environmental enrichment in rats. J Cereb Blood Flow Metab 28: 1936-1950.
81. Dahlqvist P, Rönnbäck A, Risedal A, Nergårdh R, Johansson IM, et al. (2003) Effects of postischemic environment on transcription factor and serotonin receptor expression after permanent focal cortical ischemia in rats. Neuroscience 119: 643-652. (Pubitemid 36694792)
82. Overman JJ, Carmichael ST (2014) Plasticity in the injured brain: more than molecules matter. Neuroscientist 20: 15-28.
83. Sale A, Maya Vetencourt JF, Medini P, Cenni MC, Baroncelli L, et al. (2007) Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat Neurosci 10: 679-681. (Pubitemid 46828505)
84. Foscarin S, Ponchione D, Pajaj E, Leto K, Gawlak M, et al. (2011) Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 6: e16666.
85. Katsman D, Zheng J, Spinelli K, Carmichael ST (2003) Tissue microenvironments within functional cortical subdivisions adjacent to focal stroke. J Cereb Blood Flow Metab 23: 997-1009. (Pubitemid 37082425)
86. Carmichael ST (2006) Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 59: 735-742.
87. Hill JJ, Jin K, Mao XO, Xie L, Greenberg DA (2012) Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats. Proc Natl Acad Sci U S A 109: 9155-9160.
88. Soleman S, Yip PK, Duricki DA, Moon LD (2012) Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats. Brain 135: 1210-1223.
89. Gherardini L, Gennaro M, Pizzorusso T (2013) Perilesional treatment with chondroitinase ABC and motor training promote functional recovery after stroke in rats. Cereb Cortex.
90. Lander C, Kind P, Maleski M, Hockfield S (1997) A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J Neurosci 17: 1928-1939. (Pubitemid 27106752)
91. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56: 33-42. (Pubitemid 47484182)