Refined sensory measures of neural repair in human spinal cord injury: Bridging preclinical findings to clinical value

Cell and Tissue Research

Volumn 349, Issue 1, 2012, Pages 397-404

  Haefeli, Jenny ^a   Curt, Armin ^a  

^a BALGRIST UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Contact heat evoked potentials; Neural repair; Segmental sensory assessment; Somatosensory evoked potentials; Spinal cord injury

Indexed keywords

CLINICAL ASSESSMENT TOOL; CLINICAL RESEARCH; CONVALESCENCE; DERMATOMAL CONTACT HEAT EVOKED RESPONSE; DERMATOMAL SOMATOSENSORY EVOKED RESPONSE; EVOKED SOMATOSENSORY RESPONSE; HUMAN; INTERNATIONAL STANDARDS FOR THE NEUROLOGICAL CLASSIFICATION OF SPINAL CORD INJURY; NERVE REGENERATION; NEUROLOGIC EXAMINATION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE SENSORY TESTING; REVIEW; SEGMENTAL SENSORY FUNCTION; SENSORIMOTOR FUNCTION; SENSORY FUNCTION ASSESSMENT; SENSORY NERVE CONDUCTION; SENSORY SYSTEM ELECTROPHYSIOLOGY; SPINAL CORD INJURY; SPINOTHALAMIC TRACT; TRANSLATIONAL RESEARCH;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; NEURONS; SENSATION; SPINAL CORD INJURIES; TRANSLATIONAL MEDICAL RESEARCH; WOUND HEALING;

EID: 84862742375     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1373-0     Document Type: Review

References (135)

1. Apostolova I, Irintchev A, Schachner M (2006) Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J Neurosci 30:7849-7859 (Pubitemid 44315154)
2. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438 (Pubitemid 30220330)
3. Asher RA, Scheibe RJ, Keiser HD, Bignami A (1995) On the existence of a cartilage-like proteoglycan and link proteins in the central nervous system. Glia 13:294-308
4. Aspberg A, Miura R, Bourdoulous S, Shimonaka M, Heinegârd D, Schachner M, Ruoslahti E, Yamaguchi Y (1997) The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc Natl Acad Sci USA 94(19):10116-10121 (Pubitemid 27407003)
5. Bahia CP, Houzel J-C, Picanço-Diniz CW, Pereira A Jr (2008) Spatiotemporal distribution of proteoglycans in the developing rat's barrel field and the effects of early deafferentation. J Comp Neurol 510:145-157
6. Balmer TS, Carels VM, Frisch JL, Nick TA (2009) Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci 29:12878-12885
7. Baroncelli L, Sale A, Viegi A, Maya Vetencourt JF, De Pasquale R, Baldini S, Maffei L (2010) Experience-dependent reactivation of ocular dominance plasticity in the adult visual cortex. Exp Neurol 226:100-109
8. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, McMahon SB, Bradbury EJ (2006) Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 26:10856-10867
9. Bekku Y, Su WD, Hirakawa S, Fässler R, Ohtsuka A, Kang JS, Sanders J, Murakami T, Ninomiya Y, Oohashi T (2003) Molecular cloning of Bral2, a novel brain-specific link protein and immunohistochemical colocalization with brevican in perineuronal nets. Mol Cell Neurosci 24(1):148-159 (Pubitemid 37194541)
10. Bekku Y, Vargová L, Goto Y, Vorísek I, Dmytrenko L, Narasaki M, Ohtsuka A, Fässler R, Ninomiya Y, Syková E, Oohashi T (2010) Bral1: its role in diffusion barrier formation and conduction velocity in the CNS. J Neurosci 30:3113-3123
11. Berardi N, Pizzorusso T, Ratto GM, Maffei L (2003) Molecular basis of plasticity in the visual cortex. Trends Neurosci 26:369-378 (Pubitemid 36794553)
12. Bertolotto A, Rocca G, Schiffer D (1990) Chondroitin 4-sulfate proteoglycan forms an extracellular network in human and rat central nervous system. J Neurol Sci 100:113-123
13. Bignami A, Hosley M, Dahl D (1993) Hyaluronic acid and hyaluronic acid-binding proteins in brain extracellular matrix. Anat Embryol 188:419-433 (Pubitemid 24000108)
14. Blue ME, Parnavelas JG (1983) The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. J Neurocytol 12:599-616 (Pubitemid 13043548)
15. Bradbury EJ, Carter LM (2011) Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res Bull 84:306-316
16. Bradbury EJ, Moon LDF, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640 (Pubitemid 34406764)
17. Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, Meyer H, Krug M, Böckers TM, Zhou X, Kreutz MR, Montag D, Gundelfinger ED, Fässler R (2002) Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 22:7417-7427
18. Brückner G, Brauer K, Härtig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8:183-200
19. Brückner G, Grosche J (2001) Perineuronal nets show intrinsic patterns of extracellular matrix differentiation in organotypic slice cultures. Exp Brain Res 137:83-93 (Pubitemid 32186618)
20. Brückner G, Grosche J, Schmidt S, Härtig W, Margolis RU, Delpech B, Seidenbecher CI, Czaniera R, Schachner M (2000) Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J Comp Neurol 428:616-629
21. Bukalo O, Schachner M, Dityatev A (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104:359-369 (Pubitemid 32493729)
22. Burchfiel JL, Duffy FH (1981) Role of intracortical inhibition in deprivation amblyopia: reversal by microiontophoretic bicuculline. Brain Res 206:479-484 (Pubitemid 11170231)
23. Busch SA, Silver J (2007) The role of extracellular matrix in CNS regeneration. Curr Opin Neurobiol 17(1):120-127 (Pubitemid 46227979)
24. Cafferty WBJ, Bradbury EJ, Lidierth M, Jones M, Duffy PJ, Pezet S, McMahon SB (2008) Chondroitinase ABCmediated plasticity of spinal sensory function. J Neurosci 28:11998-12009
25. Carulli D, Pizzorusso T, Kwok JCF, Putignano E, Poli A, Forostyak S andrews MR, Deepa SS, Glant TT, Fawcett JW (2010) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133:2331-2347
26. Carulli D, Rhodes KE, Brown DJ, Bonnert TP, Pollack SJ, Oliver K, Strata P, Fawcett JW (2006) Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J Comp Neurol 494:559-577 (Pubitemid 43054232)
27. Carulli D, Rhodes KE, Fawcett JW (2007) Upregulation of aggrecan, link protein 1 and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J Comp Neurol 501:83-94 (Pubitemid 46155875)
28. Celio MR, Blümcke I (1994) Perineuronal nets-a specialized form of extracellular matrix in the adult nervous system. Brain Res Brain Res Rev 19(1):128-145 (Pubitemid 24024086)
29. Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21:510-515 (Pubitemid 28555691)
30. Chang EF, Bao S, Imaizumi K, Schreiner CE, Merzenich MM (2005) Development of spectral and temporal response selectivity in the auditory cortex. Proc Natl Acad Sci USA 102:16460-16465 (Pubitemid 41688936)
31. Corvetti L, Rossi F (2005) Degradation of chondroitin sulfate proteoglycans induces sprouting of intact purkinje axons in the cerebellum of the adult rat. J Neurosci 25:7150-7158 (Pubitemid 41113931)
32. Crespo D, Asher RA, Lin R, Rhodes KE, Fawcett JW (2007) How does chondroitinase promote functional recovery in the damaged CNS? Exp Neurol 206:159-171 (Pubitemid 47094767)
33. Crook JD, Hendrickson A, Erickson A, Possin D, Robinson FR (2007) Purkinje cell axon collaterals terminate on Cat-301+ neurons in Macaca monkey cerebellum. Neuroscience 149:834-844 (Pubitemid 350122893)
34. Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, Mikami T, Sugahara K, Fawcett JW (2006) Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem 281:17789-17800 (Pubitemid 44035578)
35. Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277:43707-43716 (Pubitemid 36157787)
36. Delpech B, Delpech A, Brückner G, Girard N, Maingonnat C (1989) Hyaluronan and hyaluronectin in the nervous system. CIBA Found Symp 143:208-220, discussion 221-232, 281-285
37. Dityatev A, Brückner G, Dityateva G, Grosche J, Kleene R, Schachner M (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 67:570-588 (Pubitemid 47066941)
38. Fisher D, Xing B, Dill J, Li H, Hoang HH, Zhao Z, Yang XL, Bachoo R, Cannon S, Longo FM, Sheng M, Silver J, Li S (2011) Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 40:14051-14066
39. Foscarin S, Ponchione D, Pajaj E, Leto K, Gawlak M, Wilczynski GM, Rossi F, Carulli D (2011) Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 6:e16666
40. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12(7):897-904
41. Fry EJ, Chagnon MJ, López-Vales R, Tremblay ML, David S (2010) Corticospinal tract regeneration after spinal cord injury in receptor protein tyrosine phosphatase sigma deficient mice. Glia 58:423-433
42. Fujita SC, Tada Y, Murakami F, Hayashi M, Matsumura M (1989) Glycosaminoglycan-related epitopes surrounding different subsets of mammalian central neurons. Neurosci Res 7:117-130 (Pubitemid 20005848)
43. Galtrey CM, Asher RA, Nothias F, Fawcett JW (2007) Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 130:926-939 (Pubitemid 47355587)
44. Galtrey CM, Fawcett JW (2007) The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54:1-18 (Pubitemid 46498163)
45. Galtrey CM, Kwok JCF, Carulli D, Rhodes KE, Fawcett JW (2008) Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur J Neurosci 27:1373-1390 (Pubitemid 351406265)
46. García-Alías G, Barkhuysen S, Buckle M, Fawcett JW (2009) Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12:1145-1151
47. Gáti G, Morawski M, Lendvai D, Matthews RT, Jäger C, Zachar G, Arendt T, Alpár A (2010) Chondroitin sulphate proteoglycanbased perineuronal net establishment is largely activityindependent in chick visual system. J Chem Neuroanat 40:243-247
48. Giamanco KA, Morawski M, Matthews RT (2010) Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 170:1314-1327
49. Gogolla N, Caroni P, Lüthi A, Herry C (2009) Perineuronal nets protect fear memories from erasure. Science 325:1258-1261
50. Guimaraes 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
51. Hagihara K, Miura R, Kosaki R, Berglund E, Ranscht B, Yamaguchi Y (1999) Immunohistochemical evidence for the brevican-tenascin- R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain. J Comp Neurol 410:256-264 (Pubitemid 29323076)
52. Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T, Viegi A, Berardi N, Maffei L (2010) Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 30:361-371
53. Hardingham TE, Muir H (1972) The specific interaction of hyaluronic acid with cartillage proteoglycans. Biochim Biophys Acta 279 (2):401-405
54. Härtig W, Derouiche A, Welt K, Brauer K, Grosche J, Mäder M, Reichenbach A, Brückner G (1999) Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842:15-29
55. Härtig W, Singer A, Grosche J, Brauer K, Ottersen OP, Brückner G (2001) Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium-binding proteins and the potassium channel subunit Kv3.1b. Brain Res 899:123-133
56. Hascall VC, Heinegård D (1974) Aggregation of cartilage proteoglycans. I. The role of hyaluronic acid. J Biol Chem 249:4232-4241
57. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877-888
58. Hilbig H, Nowack S, Boeckler K, Bidmon HJ, Zilles K (2007) Characterization of neuronal subsets surrounded by perineuronal nets in the rhesus auditory brainstem. J Anat 210(5):507-517 (Pubitemid 46647819)
59. Hirakawa S, Oohashi T, Su WD, Yoshioka H, Murakami T, Arata J, Ninomiya Y (2000) The brain link protein-1 (BRAL1): cDNA cloning, genomic structure and characterization as a novel link protein expressed in adult brain. Biochem Biophys Res Commun 276:982-989
60. 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
61. Hockfield S, McKay RD (1983) A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc Natl Acad Sci USA 80:5758-5761 (Pubitemid 14249907)
62. Hockfield S, Sur M (1990) Monoclonal antibody Cat-301 identifies Ycells in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 300:320-330 (Pubitemid 20357791)
63. Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609-652
64. Ishiguro H, Sato S, Fujita N, Inuzuka T, Nakano R, Miyatake T (1991) Immunohistochemical localization of myelin-associated glycoprotein isoforms during the development in the mouse brain. Brain Res 563:288-292
65. Iwai Y, Fagiolini M, Obata K, Hensch TK (2003) Rapid critical period induction by tonic inhibition in visual cortex. J Neurosci 23:6695-6702 (Pubitemid 36951197)
66. John N, Krügel H, Frischknecht R, Smalla KH, Schultz C, Kreutz MR, Gundelfinger ED, Seidenbecher CI (2006) Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol Cell Neurosci 31(4):774-784
67. Kalb R, Hockfield S (1988) Molecular evidence for early activity-dependent development of hamster motor neurons. J Neurosci 8:2350-2360
68. Kalb RG, Hockfield S (1994) Electrical activity in the neuromuscular unit can influence the molecular development of motor neurons. Dev Biol 162:539-548 (Pubitemid 24144129)
69. Kaliszewska A, Bijata M, Kaczmarek L, Kossut M (2011) Experience-dependent plasticity of the barrel cortex in mice observed with 2-DG brain mapping and c-Fos: effects of MMP-9 KO. Cereb Cortex Oct 20 [Epub ahead of print]
70. Kind PC, Beaver CJ, Mitchell DE (1995) Effects of early periods of monocular deprivation and reverse lid suture on the development of Cat-301 immunoreactivity in the dorsal lateral geniculate nucleus (dLGN) of the cat. J Comp Neurol 359:523-536
71. Knudson CB, KnudsonW(1993) Hyaluronan-binding proteins in development, tissue homeostasis and disease. FASEB J 7(13):1233-1241 (Pubitemid 23314358)
72. Köppe G, Brückner G, Härtig W, Delpech B, Bigl V (1997) Characterization of proteoglycan-containing perineuronal nets by enzymatic treatments of rat brain sections. Histochem J 29(1):11-20 (Pubitemid 27173644)
73. Kwok JC, Afshari F, García-Alías G, Fawcett JW (2008) Proteoglycans in the central nervous system: plasticity, regeneration and their stimulation with chondroitinase ABC. Restor Neurol Neurosci 26(2-3):131-145
74. Kwok JCF, Carulli D, Fawcett JW (2010) In vitro modeling of perineuronal nets: hyaluronan synthase and link protein are necessary for their formation and integrity. J Neurochem 114:1447-1459
75. Kwok JCF, Dick G, Wang D, Fawcett JW (2011) Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol 71(11):1073-1089. Available at: http://www.ncbi.nlm.nih.gov/pubmed/21898855 [Accessed September 10, 2011]
76. Lafarga M, Berciano MT, Blanco M (1984) The perineuronal net in the fastigial nucleus of the rat cerebellum. A Golgi and quantitative study. Anat Embryol 170:79-85 (Pubitemid 14097725)
77. Lander C, Kind P, Maleski M, Hockfield S (1997) A family of activitydependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J Neurosci 17:1928-1939 (Pubitemid 27106752)
78. Lien CC, Jonas P (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J Neurosci 23(6):2058-2068
79. Lundell A, Olin AI, Mörgelin M, al-Karadaghi S, Aspberg A, Logan DT (2004) Structural basis for interactions between tenascins and lectican C-type lectin domains: evidence for a crosslinking role for tenascins. Structure 12:1495-1506 (Pubitemid 39092094)
80. Mabuchi M, Murakami S, Taguchi T, Ohtsuka A, Murakami T (2001) Purkinje cells in the adult cat cerebellar cortex possess a perineuronal net of proteoglycans. Arch Histol Cytol 64:203-209 (Pubitemid 32578442)
81. Maeda N, Hamanaka H, Oohira A, Noda M (1995) Purification, characterization and developmental expression of a brain-specific chondroitin sulfate proteoglycan, 6B4 proteoglycan/phosphacan. Neuroscience 67:23-35
82. Maffei A, Nataraj K, Nelson SB, Turrigiano GG (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443:81-84 (Pubitemid 44344051)
83. Marks MS, Chi-Rosso G, Toole BP (1990) Hyaluronate-binding proteins of murine brain. J Neurochem 54:171-180
84. Massey JM, Hubscher CH,Wagoner MR, Decker JA, Amps J, Silver J, Onifer SM (2006) Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26:4406-4414 (Pubitemid 44315399)
85. Matsui F, Nishizuka M, Yasuda Y, Aono S, Watanabe E, Oohira A (1998) Occurrence of a N-terminal proteolytic fragment of neurocan, not a C-terminal half, in a perineuronal net in the adult rat cerebrum. Brain Res 790:45-51 (Pubitemid 28234486)
86. McKeon RJ, Jurynec MJ, Buck CR (1999) The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci 19:10778-10788 (Pubitemid 30235724)
87. 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)
88. Meyer K, Linker A, Rapport MM (1951) The production of monosaccharides from hyaluronic acid by beta-glucuronidase. J Biol Chem 192:275-281
89. Meyer-Puttlitz B, Junker E, Margolis RU, Margolis RK (1996) Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan. J Comp Neurol 366:44-54 (Pubitemid 26069849)
90. Mikami T, Yasunaga D, Kitagawa H (2009) Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J Biol Chem 284:4494-4499
91. Morales B, Choi S-Y, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22:8084-8090 (Pubitemid 35379114)
92. Nakagawa F, Schulte BA, Spicer SS (1986) Selective cytochemical demonstration of glycoconjugate-containing terminal N-acetylgalactosamine on some brain neurons. J Comp Neurol 243:280-290 (Pubitemid 16175100)
93. Nakamura M, Nakano K, Morita S, Nakashima T, Oohira A, Miyata S (2009) Expression of chondroitin sulfate proteoglycans in barrel field of mouse and rat somatosensory cortex. Brain Res 1252:117-129
94. Neame PJ, Christner JE, Baker JR (1986) The primary structure of link protein from rat chondrosarcoma proteoglycan aggregate. J Biol Chem 261:3519-3535
95. Niederöst BP, Zimmermann DR, Schwab ME, Bandtlow CE (1999) Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J Neurosci 19:8979-8989 (Pubitemid 30226718)
96. Nowicka D, Soulsby S, Skangiel-Kramska J, Glazewski S (2009) Parvalbumin-containing neurons, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur J Neurosci 30:2053-2063
97. Oohashi T, Hirakawa S, Bekku Y, Rauch U, Zimmermann DR, Su W-D, Ohtsuka A, Murakami T, Ninomiya Y (2002) Bral1, a brain-specific link protein, colocalizing with the versican V2 isoform at the nodes of Ranvier in developing and adult mouse central nervous systems. Mol Cell Neurosci 19:43-57 (Pubitemid 34113696)
98. Oohira A, Matsui F, Katoh-Semba R (1991) Inhibitory effects of brain chondroitin sulfate proteoglycans on neurite outgrowth from PC12D cells. J Neurosci 11:822-827
99. Oohira A, Matsui F, Watanabe E, Kushima Y, Maeda N (1994) Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience 60:145-157 (Pubitemid 24147614)
100. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248-1251 (Pubitemid 35285495)
101. Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L (2006) Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci USA 103:8517-8522 (Pubitemid 43838487)
102. Quirk GJ, Paré D, Richardson R, Herry C, Monfils MH, Schiller D, Vicentic A (2010) Erasing fear memories with extinction training. J Neurosci 30:14993-14997
103. Rauch U, Hirakawa S, Oohashi T, Kappler J, Roos G (2004) Cartilage link protein interacts with neurocan, which shows hyaluronan binding characteristics different from CD44 and TSG-6. Matrix Biol 22(8):629-639 (Pubitemid 38520092)
104. Reimers S, Hartlage-Rübsamen M, Brückner G, Rossner S (2007) Formation of perineuronal nets in organotypic mouse brain slice cultures is independent of neuronal glutamatergic activity. Eur J Neurosci 25:2640-2648 (Pubitemid 46888830)
105. Ruoslahti E (1996) Brain extracellular matrix. Glycobiology 6:489-492
106. Saghatelyan AK, Dityatev A, Schmidt S, Schuster T, Bartsch U, Schachner M (2001) Reduced perisomatic inhibition, increased excitatory transmission and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol Cell Neurosci 17:226-240 (Pubitemid 32113549)
107. Sale A, Berardi N, Spolidoro M, Baroncelli L, Maffei L (2010) GABAergic inhibition in visual cortical plasticity. Front Cell Neurosci 4:10
108. Sale A, Maya Vetencourt JF, Medini P, Cenni MC, Baroncelli L, De Pasquale R, Maffei L (2007) Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat Neurosci 10:679-681 (Pubitemid 46828505)
109. Schweizer M, Streit WJ, Müller CM (1993) Postnatal development and localization of an N-acetylgalactosamine containing glycoconjugate associated with nonpyramidal neurons in cat visual cortex. J Comp Neurol 329:313-327 (Pubitemid 23078227)
110. Seeger G, Brauer K, Härtig W, Brückner G (1994) Mapping of perineuronal nets in the rat brain stained by colloidal iron hydroxide histochemistry and lectin cytochemistry. Neuroscience 58:371-388 (Pubitemid 24037248)
111. Sengpiel F, Price DN, Vorobyov V, Fawcett JW (2008) Effects of digestion of extracellular matrix molecules on plasticity in cat primary visual cortex. 2008 Neuroscience Meeting Planner Program No. 9.7. Society for Neuroscience, Washington, DC. Online
112. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596
113. Snow DM, Brown EM, Letourneau PC (1996) Growth cone behavior in the presence of soluble chondroitin sulfate proteoglycan (CSPG), compared to behavior on CSPG bound to laminin or fibronectin. Int J Dev Neurosci 14:331-349 (Pubitemid 26238175)
114. Spicer AP, Joo A, Bowling RA Jr (2003) A hyaluronan binding link protein gene family whose members are physically linked adjacent to chondroitin sulfate proteoglycan core protein genes: the missing links. J Biol Chem 278:21083-21091 (Pubitemid 36806420)
115. Spolidoro M, Sale A, Berardi N, Maffei L (2009) Plasticity in the adult brain: lessons from the visual system. Exp Brain Res 192:335-341
116. Steindler DA, Cooper NG, Faissner A, Schachner M (1989) Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol 131:243-260 (Pubitemid 19032142)
117. Sur M, Frost D, Hockfield S (1988) Expression of a surface-associated antigen on Y-cells in the cat lateral geniculate nucleus is regulated by visual experience. J Neurosci 8:874-882 (Pubitemid 18085157)
118. Tom VJ, Kadakia R, Santi L, Houlé JD (2009) Administration of chondroitinase ABC rostral or caudal to a spinal cord injury site promotes anatomical but not functional plasticity. J Neurotrauma 26:2323-2333
119. Toole BP (2000) Hyaluronan is not just a goo! J Clin Invest 106:335-336
120. Tropea D, Caleo M, Maffei L (2003) Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. J Neurosci 23:7034-7044 (Pubitemid 36975869)
121. Tsifrina E, Ananyeva NM, Hastings G, Liau G (1999) Identification and characterization of three cDNAs that encode putative novel hyaluronan-binding proteins, including an endothelial cell-specific hyaluronan receptor. Am J Pathol 155:1625-1633
122. Vitellaro-Zuccarello L, Bosisio P, Mazzetti S, Monti C, De Biasi S (2007) Differential expression of several molecules of the extracellular matrix in functionally and developmentally distinct regions of rat spinal cord. Cell Tissue Res 327(3):433-447 (Pubitemid 46232314)
123. Vo T, Carulli D, Ehlert EME, Kwok JCF, Asher RA, Fawcett JW, Verhaagen J (2007) The chemorepulsive axon guidance protein Semaphorin 3A is a constituent of perineuronal nets in the adult rodent brain. 2007 Neuroscience Meeting Planner Program No. 585.1/Q17. Society for Neuroscience, San Diego. Online
124. Wang D, Ichiyama RM, Zhao R andrews MR, Fawcett JW (2011) Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31:9332-9344
125. Watanabe E, Maeda N, Matsui F, Kushima Y, Noda M, Oohira A (1995) Neuroglycan C, a novel membrane-spanning chondroitin sulfate proteoglycan that is restricted to the brain. J Biol Chem 270:26876-26882
126. Watanabe K, Oohira A, Katoh-Semba R, Totsuka T, Yoshida K (1989) Sulfated proteoglycans synthesized by Neuro 2a neuroblastoma cells: comparison between cells with and without ganglioside-induced neurites. Neurochem Res 14:707-716 (Pubitemid 19255824)
127. Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, Margolis RU, Levinson SR, Shrager P, Montag D, Schachner M (1999) Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 19:4245-4262 (Pubitemid 29241079)
128. Wegner F, Härtig W, Bringmann A, Grosche J,Wohlfarth K, Zuschratter W, Brückner G (2003) Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABA(A) receptor alpha1 subunit form a unique entity in rat cerebral cortex. Exp Neurol 184(2):705-714 (Pubitemid 38182799)
129. Williams ME, de Wit J, Ghosh A (2010) Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron 68:9-18
130. De Wit J, De Winter F, Klooster J, Verhaagen J (2005) Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol Cell Neurosci 29:40-55 (Pubitemid 40603879)
131. Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57:276-289
132. Yin ZQ, Crewther SG, Wang C, Crewther DP (2006) Pre- and post-critical period induced reduction of Cat-301 immunoreactivity in the lateral geniculate nucleus and visual cortex of cats Y-blocked as adults or made strabismic as kittens. Mol Vis 12:858-866 (Pubitemid 44184720)
133. Yuan W, Matthews RT, Sandy JD, Gottschall PE (2002) Association between protease-specific proteolytic cleavage of brevican and synaptic loss in the dentate gyrus of kainate-treated rats. Neuroscience 114:1091-1101
134. Zaremba S, Guimaraes A, Kalb RG, Hockfield S (1989) Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 2:1207-1219
135. Zimmermann DR, Dours-Zimmermann MT (2008) Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 130:635-653