Molecular composition of extracellular matrix in the vestibular nuclei of the rat

Brain Structure and Function

Volumn 219, Issue 4, 2014, Pages 1385-1403

  Rácz, Éva ^a   Gaál, Botond ^a   Kecskes, Szilvia ^a   Matesz, Clara ^a,b  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Brainstem; Chondroitin sulfate proteoglycans; Hyaluronan; Link protein; Perineuronal net; Tenascin R; Vestibular system

Indexed keywords

AGGRECAN; BREVICAN; HAPLN1 PROTEIN; HYALURONIC ACID; LINK PROTEIN; NEUROCAN; TENASCIN; UNCLASSIFIED DRUG; VERSICAN; PROTEOGLYCAN; SCLEROPROTEIN; TENASCIN R;

ADULT; ANALYTICAL PARAMETERS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOARCHITECTURE; EXTRACELLULAR MATRIX; FEMALE; IMMUNOHISTOCHEMISTRY; LATERAL VESTIBULAR NUCLEUS; MEDIAL VESTIBULAR NUCLEUS; MOLECULAR COMPOSITION; MOLECULE; NONHUMAN; PRIORITY JOURNAL; RAT; STAINING; SUPERIOR VESTIBULAR NUCLEUS; ANIMAL; METABOLISM; NERVE CELL; NEUROPIL; VESTIBULAR NUCLEUS; WISTAR RAT;

RATTUS;

AGGRECANS; ANIMALS; BREVICAN; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HYALURONIC ACID; NEUROCAN; NEURONS; NEUROPIL; PROTEOGLYCANS; RATS; RATS, WISTAR; TENASCIN; VESTIBULAR NUCLEI;

EID: 84904284569     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0575-x     Document Type: Article

References (111)

1. Afshari FT, Kwok JC, White L, Fawcett JW (2010) Schwann cell migration is integrin-dependent and inhibited by astrocyte-produced aggrecan. Glia 58(7):857-869
2. Ajmo JM, Eakin AK, Hamel MG, Gottschall PE (2008) Discordant localization of WFA reactivity and brevican/ADAMTS-derived fragment in rodent brain. BMC Neurosci 9:14
3. 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(7):2427-2438 (Pubitemid 30220330)
4. Asher RA, Morgenstern DA, Shearer MC, Adcock KH, Pesheva P, Fawcett JW (2002) Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J Neurosci 22(6):2225-2236 (Pubitemid 35386522)
5. Babalian AL, Vidal PP (2000) Floccular modulation of vestibuloocular pathways and cerebellum-related plasticity: an in vitro whole brain study. J Neurophysiol 84(5):2514-2528
6. Babalian A, Vibert N, Assie G, Serafin M, Muhlethaler M, Vidal PP (1997) Central vestibular networks in the guinea-pig: functional characterization in the isolated whole brain in vitro. Neuroscience 81(2):405-426 (Pubitemid 27381997)
7. Bacskai T, Szekely G, Matesz C (2002) Ascending and descending projections of the lateral vestibular nucleus in the rat. Acta Biol Hung 53(1-2):7-21 (Pubitemid 34414092)
8. Bagnall MW, Stevens RJ, du Lac S (2007) Transgenic mouse lines subdivide medial vestibular nucleus neurons into discrete, neurochemically distinct populations. J Neurosci 27(9):2318-2330 (Pubitemid 46340951)
9. Balaban CD (1996) Vestibular nucleus projections to the parabrachial nucleus in rabbits: implications for vestibular influences on the autonomic nervous system. Exp Brain Res 108(3):367-381
10. Bekku Y, Rauch U, Ninomiya Y, Oohashi T (2009) Brevican distinctively assembles extracellular components at the large diameter nodes of Ranvier in the CNS. J Neurochem 108(5):1266-1276
11. Bekku Y, Vargova L, Goto Y, Vorisek I, Dmytrenko L, Narasaki M, Ohtsuka A, Fassler R, Ninomiya Y, Sykova E, Oohashi T (2010) Bral1: its role in diffusion barrier formation and conduction velocity in the CNS. J Neurosci 30(8):3113-3123
12. Bertolotto A, Manzardo E, Guglielmone R (1996) Immunohistochemical mapping of perineuronal nets containing chondroitin unsulfated proteoglycan in the rat central nervous system. Cell Tissue Res 283(2):283-295 (Pubitemid 26040878)
13. Bignami A, Hosley M, Dahl D (1993) Hyaluronic acid and hyaluronic acid-binding proteins in brain extracellular matrix. Anat Embryol (Berl) 188(5):419-433 (Pubitemid 24000108)
14. Birinyi A, Straka H, Matesz C, Dieringer N (2001) Location of dye-coupled second order and of efferent vestibular neurons labeled from individual semicircular canal or otolith organs in the frog. Brain Res 921(1-2):44-59 (Pubitemid 33096283)
15. Blosa M, Sonntag M, Bruckner G, Jager C, Seeger G, Matthews RT, Rubsamen R, Arendt T, Morawski M (2013) Unique features of extracellular matrix in the mouse medial nucleus of trapezoid body - implications for physiological functions. Neuroscience 228:215-234
16. Brodal P, Brodal A (1981) The olivocerebellar projection in the monkey. Experimental studies with the method of retrograde tracing of horseradish peroxidase. J Comp Neurol 201(3):375-393 (Pubitemid 11010910)
17. Brown JE, Card JP, Yates BJ (2005) Polysynaptic pathways from the vestibular nuclei to the lateral mammillary nucleus of the rat: substrates for vestibular input to head direction cells. Exp Brain Res 161(1):47-61 (Pubitemid 40238869)
18. Bruckner G, Grosche J, Schmidt S, Hartig 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(4):616-629
19. Bruckner G, Morawski M, Arendt T (2008) Aggrecan-based extracellular matrix is an integral part of the human basal ganglia circuit. Neuroscience 151(2):489-504
20. Camp AJ, Callister RJ, Brichta AM (2006) Inhibitory synaptic transmission differs in mouse type A and B medial vestibular nucleus neurons in vitro. J Neurophysiol 95(5):3208-3218
21. 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(4):559-577 (Pubitemid 43054232)
22. 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(1):83-94 (Pubitemid 46155875)
23. Carulli D, Pizzorusso T, Kwok JC, 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(Pt 8):2331-2347
24. Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21(12): 510-515 (Pubitemid 28555691)
25. Costa C, Tortosa R, Domenech A, Vidal E, Pumarola M, Bassols A (2007) Mapping of aggrecan, hyaluronic acid, heparan sulphate proteoglycans and aquaporin 4 in the central nervous system of the mouse. J Chem Neuroanat 33(3):111-123 (Pubitemid 46528688)
26. Deak A, Bacskai T, Gaal B, Racz E, Matesz K (2012) Effect of unilateral labyrinthectomy on the molecular composition of perineuronal nets in the lateral vestibular nucleus of the rat. Neurosci Lett 513(1):1-5
27. 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(26):17789-17800 (Pubitemid 44035578)
28. Delpech B, Delpech A, Bruckner G, Girard N, Maingonnat C (1989) Hyaluronan and hyaluronectin in the nervous system. Ciba Found Symp 143:208-220
29. Díaz C, Glover JC, Puelles L, Bjaalie JG (2003) The relationship between hodological and cytoarchitectonic organization in the vestibular complex of the 11-day chicken embryo. J Comp Neurol 457(1):87-105 (Pubitemid 36172575)
30. Dityatev A, Fellin T (2008) Extracellular matrix in plasticity and epileptogenesis. Neuron Glia Biol 4(3):235-247
31. Dityatev A, Rusakov DA (2010) Molecular signals of plasticity at the tetrapartite synapse. Curr Opin Neurobiol 21(2):353-359
32. Dityatev A, Schachner M (2003) Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 4(6):456-468 (Pubitemid 37280167)
33. Dityatev A, Schachner M (2006) The extracellular matrix and synapses. Cell Tissue Res 326(2):647-654 (Pubitemid 44435831)
34. du Lac S, Lisberger SG (1995) Membrane and firing properties of avian medial vestibular nucleus neurons in vitro. J Comp Physiol A 176(5):641-651
35. Eggli PS, Lucocq J, Ott P, Graber W, van der Zypen E (1992) Ultrastructural localization of hyaluronan in myelin sheaths of the rat central and rat and human peripheral nervous systems using hyaluronan-binding protein-gold and link protein-gold. Neuroscience 48(3):737-744
36. Eugene D, Idoux E, Beraneck M, Moore LE, Vidal PP (2011) Intrinsic membrane properties of central vestibular neurons in rodents. Exp Brain Res 210(3-4):423-436
37. Frischknecht R, Seidenbecher CI (2012) Brevican: a key proteoglycan in the perisynaptic extracellular matrix of the brain. Int J Biochem Cell Biol 44(7):1051-1054
38. 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
39. Gacek RR (1969) The course and central termination of first order neurons supplying vestibular endorgans in the cat. Acta Otolaryngol Suppl 254:1-66
40. Gati G, Morawski M, Lendvai D, Jager C, Negyessy L, Arendt T, Alpar A (2010) Distribution and classification of aggrecan-based extracellular matrix in the thalamus of the rat. J Neurosci Res 88(15):3257-3266
41. Giamanco KA, Morawski M, Matthews RT (2010) Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 170(4):1314-1327
42. Gong Q, Bailey MS, Pixley SK, Ennis M, Liu W, Shipley MT (1994) Localization and regulation of low affinity nerve growth factor receptor expression in the rat olfactory system during development and regeneration. J Comp Neurol 344(3):336-348 (Pubitemid 24177221)
43. Hagihara K, Miura R, Kosaki R, Berglund E, Ranscht B, Yamaguchi Y (1999) Immunohistochemical evidence for the brevicantenascin-R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain. J Comp Neurol 410(2):256-264 (Pubitemid 29323076)
44. Hartig W, Brauer K, Bruckner G (1992) Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. NeuroReport 3(10):869-872
45. Hartig W, Derouiche A, Welt K, Brauer K, Grosche J, Mader M, Reichenbach A, Bruckner 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(1):15-29 (Pubitemid 29447848)
46. Hartig W, Singer A, Grosche J, Brauer K, Ottersen OP, Bruckner 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(1-2):123-133 (Pubitemid 32324153)
47. Highstein SM (1971) Organization of the inhibitory and excitatory vestibulo-ocular reflex pathways to the third and fourth nuclei in rabbit. Brain Res 32(1):218-224
48. 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)
49. Holstein GR, Friedrich VL Jr, Kang T, Kukielka E, Martinelli GP (2011) Direct projections from the caudal vestibular nuclei to the ventrolateral medulla in the rat. Neuroscience 175:104-117
50. Ito M, Highstein SM, Tsuchiya T (1970) The postsynaptic inhibition of rabbit oculomotor neurones by secondary vestibular impulses and its blockage by picrotoxin. Brain Res 17(3):520-523
51. Jian BJ, Acernese AW, Lorenzo J, Card JP (1044) Yates BJ (2005) Afferent pathways to the region of the vestibular nuclei that participates in cardiovascular and respiratory control. Brain Res 2:241-250 (Pubitemid 40693456)
52. Johnston AR, MacLeod NK, Dutia MB (1994) Ionic conductances contributing to spike repolarization and after-potentials in rat medial vestibular nucleus neurones. J Physiol 481(Pt 1):61-77 (Pubitemid 24361348)
53. Kerman IA, Shabrang C, Taylor L, Akil H, Watson SJ (2006) Relationship of presympathetic-premotor neurons to the serotonergic transmitter system in the rat brainstem. J Comp Neurol 499(6):882-896 (Pubitemid 44892816)
54. Kodama T, Guerrero S, Shin M, Moghadam S, Faulstich M, du Lac S (2012) Neuronal classification and marker gene identification via single-cell expression profiling of brainstem vestibular neurons subserving cerebellar learning. J Neurosci 32(23):7819-7831
55. Kolkman KE, Moghadam SH, du Lac S (2011) Intrinsic physiology of identified neurons in the prepositus hypoglossi and medial vestibular nuclei. J Vestib Res 21(1):33-47
56. Koppe G, Bruckner G, Brauer K, Hartig W, Bigl V (1997) Developmental patterns of proteoglycan-containing extracellular matrix in perineuronal nets and neuropil of the postnatal rat brain. Cell Tissue Res 288(1):33-41 (Pubitemid 27136141)
57. Kwok JC, 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(5):1447-1459
58. Ladpli R, Brodal A (1968) Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. Brain Res 8(1):65-96
59. Lendvai D, Morawski M, Bruckner G, Negyessy L, Baksa G, Glasz T, Patonay L, Matthews RT, Arendt T, Alpar A (2012) Perisynaptic aggrecan-based extracellular matrix coats in the human lateral geniculate body devoid of perineuronal nets. J Neurosci Res 90(2):376-387
60. Lendvai D, Morawski M, Négyessy L, Gáti G, Jäger C, Baksa G, Glasz T, Attems J, Tanila H, Arendt T, Harkany T, Alpár A (2013) Neurochemical mapping of the human hippocampus reveals perisynaptic matrix around functional synapses in Alzheimer's disease. Acta Neuropathol 125(2):215-229
61. Margolis RK, Margolis RU, Preti C, Lai D (1975) Distribution and metabolism of glycoproteins and glycosaminoglycans in subcellular fractions of brain. Biochemistry 14(22):4797-4804
62. Matesz C (1988) Fine structure of the primary afferent vestibulocochlear terminals in the frog. Acta Biol Hung 39(2-3):267-277
63. Matesz C, Nagy E, Kulik A, Tonkol A (1997) Projections of the medial and superior vestibular nuclei to the brainstem and spinal cord in the rat. Neurobiology (Bp) 5(4):489-493 (Pubitemid 29111505)
64. Matesz C, Modis L, Halasi G, Szigeti ZM, Felszeghy S, Bacskai T, Szekely G (2005) Extracellular matrix molecules and their possible roles in the regeneration of frog nervous system. Brain Res Bull 66(4-6):526-531 (Pubitemid 41247707)
65. McCall AA, Yates BJ (2011) Compensation following bilateral vestibular damage. Front Neurol 2:88
66. McCrea RA, Strassman A, Highstein SM (1987a) Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey. J Comp Neurol 264(4):571-594 (Pubitemid 17159470)
67. McCrea RA, Strassman A, May E, Highstein SM (1987b) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264(4):547-570 (Pubitemid 17159469)
68. Meszar Z, Felszeghy S, Veress G, Matesz K, Szekely G, Modis L (2008) Hyaluronan accumulates around differentiating neurons in spinal cord of chicken embryos. Brain Res Bull 75(2-4):414-418 (Pubitemid 351335157)
69. Midura RJ, Su X, Morcuende JA, Tammi M, Tammi R (2003) Parathyroid hormone rapidly stimulates hyaluronan synthesis by periosteal osteoblasts in the tibial diaphysis of the growing rat. J Biol Chem 278(51):51462-51468 (Pubitemid 38020387)
70. Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU (1998) Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247(2):207-212 (Pubitemid 28420801)
71. Mitsacos A, Reisine H, Highstein SM (1983a) The superior vestibular nucleus: an intracellular HRP study in the cat. I. Vestibuloocular neurons. J Comp Neurol 215(1):78-91 (Pubitemid 13127270)
72. Mitsacos A, Reisine H, Highstein SM (1983b) The superior vestibular nucleus: an intracellular HRP study in the cat. II. Non-vestibuloocular neurons. J Comp Neurol 215(1):92-107 (Pubitemid 13127271)
73. Morawski M, Bruckner G, Jager C, Seeger G, Kunzle H, Arendt T (2010) Aggrecan-based extracellular matrix shows unique cortical features and conserved subcortical principles of mammalian brain organization in the Madagascan lesser hedgehog tenrec (Echinops telfairi Martin. Neuroscience 165(3):831-849
74. Morawski M, Bruckner G, Jager C, Seeger G, Matthews RT, Arendt T (2012) Involvement of perineuronal and perisynaptic extracellular matrix in Alzheimer's disease neuropathology. Brain Pathol 22(4):547-561
75. Morita S, Oohira A, Miyata S (2010) Activity-dependent remodeling of chondroitin sulfate proteoglycans extracellular matrix in the hypothalamo-neurohypophysial system. Neuroscience 166(4):1068-1082
76. Oohashi T, Hirakawa S, Bekku Y, Rauch U, Zimmermann DR, Su WD, 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(1):43-57 (Pubitemid 34113696)
77. Pasqualetti M, Díaz C, Renaud JS, Rijli FM, Glover JC (2007) Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo. J Neurosci 27(36):9670-9681 (Pubitemid 47492178)
78. Paxinos G, Watson Ch (1998) The rat brain - in stereotaxic coordinates. Academic Press, San Diego
79. Pesheva P, Probstmeier R (2000) The yin and yang of tenascin-R in CNS development and pathology. Prog Neurobiol 61(5):465-493 (Pubitemid 30169055)
80. Peusner KD, Lindberg NH, Mansfield PF (1988) Ultrastructural study of calycine synaptic endings of colossal vestibular fibers in the cristae ampullares of the developing chick. Int J Dev Neurosci 6(3):267-283
81. Pompeiano O, Brodal A (1957) Spinovestibular fibers in the cat; an experimental study. J Comp Neurol 108(3):353-381
82. Porter JD, Balaban CD (1997) Connections between the vestibular nuclei and brain stem regions that mediate autonomic function in the rat. J Vestib Res 7(1):63-76 (Pubitemid 27145572)
83. Ruggiero DA, Mtui EP, Otake K, Anwar M (1996) Vestibular afferents to the dorsal vagal complex: substrate for vestibular-autonomic interactions in the rat. Brain Res 743(1-2):294-302 (Pubitemid 27028784)
84. Ruigrok TJH, Voogd J (1990) Cerebellar nucleo-olivary projections in the rat: an anterograde tracing study with Phaseolus vulgaris leucoagglutinin (PHA-L). J Comp Neurol 298:315-333
85. Saito Y, Takazawa T, Ozawa S (2008) Relationship between afterhyperpolarization profiles and the regularity of spontaneous firings in rat medial vestibular nucleus neurons. Eur J Neurosci 28(2):288-298
86. Schmalfeldt M, Bandtlow CE, Dours-Zimmermann MT, Winterhalter KH, Zimmermann DR (2000) Brain derived versican V2 is a potent inhibitor of axonal growth. J Cell Sci 113(Pt 5):807-816 (Pubitemid 30168649)
87. Sekirnjak C, du Lac S (2006) Physiological and anatomical properties of mouse medial vestibular nucleus neurons projecting to the oculomotor nucleus. J Neurophysiol 95(5):3012-3023
88. Sekirnjak C, Vissel B, Bollinger J, Faulstich M, du Lac S (2003) Purkinje cell synapses target physiologically unique brainstem neurons. J Neurosci 23(15):6392-6398 (Pubitemid 36875642)
89. Serafin M, de Waele C, Khateb A, Vidal PP, Muhlethaler M (1991) Medial vestibular nucleus in the guinea-pig. I. Intrinsic membrane properties in brainstem slices. Exp Brain Res 84(2):417-425
90. Shin BS, Oh SY, Kim JS, Kim TW, Seo MW, Lee H, Park YA (2011) Cervical and ocular vestibular-evoked myogenic potentials in acute vestibular neuritis. Clin Neurophysiol 123(2):369-375
91. Shinder ME, Taube JS (2010) Differentiating ascending vestibular pathways to the cortex involved in spatial cognition. J Vestib Res 20(1):3-23
92. Shiroyama T, Kayahara T, Yasui Y, Nomura J, Nakano K (1999) Projections of the vestibular nuclei to the thalamus in the rat: a Phaseolus vulgaris leucoagglutinin study. J Comp Neurol 407(3):318-332 (Pubitemid 29191193)
93. Sotelo C, Palay SL (1970) The fine structure of the later vestibular nucleus in the rat. II. Synaptic organization. Brain Res 18(1):93-115
94. Stein BM, Carpenter MB (1967) Central projections of portions of vestibular ganglia innervating specific parts of the labyrinth in the rhesus monkey. Am J Anat 120:281-318
95. Straka H, Vibert N, Vidal PP, Moore LE, Dutia MB (2005) Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog Neurobiol 76(6):349-392 (Pubitemid 41636777)
96. Suarez C, Gonzalez del Rey C, Tolivia J, Llorente JL, Diaz C, Navarro A, Gomez J (1993) Morphometric analysis of the vestibular complex in the rat. Laryngoscope 103(7):762-773 (Pubitemid 23207078)
97. Sykova E, Nicholson C (2008) Diffusion in brain extracellular space. Physiol Rev 88(4):1277-1340
98. Szigeti ZM, Matesz C, Szekely G, Felszeghy S, Bacskai T, Halasi G, Meszar Z,Modis L (2006) Distribution of hyaluronan in the central nervous system of the frog. J Comp Neurol 496(6):819-831
99. Takazawa T, Saito Y, Tsuzuki K, Ozawa S (2004) Membrane and firing properties of glutamatergic and GABAergic neurons in the rat medial vestibular nucleus. J Neurophysiol 92(5):3106-3120 (Pubitemid 40340516)
100. Uno A, Idoux E, Beraneck M, Vidal PP, Moore LE, Wilson VJ, Vibert N (2003) Static and dynamic membrane properties of lateral vestibular nucleus neurons in guinea pig brain stem slices. J Neurophysiol 90(3):1689-1703 (Pubitemid 37129378)
101. 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)
102. Voogd J (1964) The cerebellum of the cat. Structure and fiber connections. Thesis, Van Gorcum, Assen
103. Voogd J, Epema AH, Rubertone JA (1991) Cerebello-vestibular connections of the anterior vermis. A retrograde tracer study in different mammals including primates. Arch Ital Biol 129(1):3-19
104. Voustianiouk A, Kaufmann H, Diedrich A, Raphan T, Biaggioni I, Macdougall H, Ogorodnikov D, Cohen B (2006) Electrical activation of the human vestibulo-sympathetic reflex. Exp Brain Res 171(2):251-261
105. Wang D, Fawcett J (2012) The perineuronal net and the control of CNS plasticity. Cell Tissue Res 349(1):147-160
106. Wegner F, Hartig W, Bringmann A, Grosche J, Wohlfarth K, Zuschratter W, Bruckner 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)
107. Yamada H, Fredette B, Shitara K, Hagihara K, Miura R, Ranscht B, Stallcup WB, Yamaguchi Y (1997) The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J Neurosci 17(20):7784-7795 (Pubitemid 27426216)
108. Yamaguchi Y (1996) Brevican: a major proteoglycan in adult brain. Perspect Dev Neurobiol 3(4):307-317
109. Yasuhara O, Akiyama H, McGeer EG, McGeer PL (1994) Immunohistochemical localization of hyaluronic acid in rat and human brain. Brain Res 635(1-2):269-282 (Pubitemid 24031413)
110. Yates BJ, Balaban CD, Miller AD, Endo K, Yamaguchi Y (1995) Vestibular inputs to the lateral tegmental field of the cat: potential role in autonomic control. Brain Res 689(2):197-206
111. Zimmermann DR, Dours-Zimmermann MT (2008) Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 130(4):635-653