Expression of calcium-binding proteins and nNOS in the human vestibular and precerebellar brainstem

Journal of Comparative Neurology

Volumn 518, Issue 6, 2010, Pages 872-895

  Baizer, Joan S ^a   Broussard, Dianne M ^b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Mossy fibers; Otoliths; Semicircular canals; Vestibular nuclear complex; Vestibulospinal tracts

Indexed keywords

ANTIBODY; ANTIGEN; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; NEURONAL NITRIC OXIDE SYNTHASE; PARVALBUMIN;

ADULT; AGED; ANTIGEN RETRIEVAL; ARTICLE; BRAIN STEM; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NEUROCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; VESTIBULAR NUCLEUS;

AGED; BRAIN STEM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CALCIUM-BINDING PROTEINS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE I; PARVALBUMINS; SPECIES SPECIFICITY;

EID: 77949393608     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22250     Document Type: Article

References (107)

1. Akaike T. 1983. Neuronal organization of the vestibulospinal system in the cat. Brain Res 259:217-227.
2. Alvarez JC, Diaz C, Suarez C, Fernandez JA, Gonzalez del Rey C, Navarro A, Tolivia J. 1998. Neuronal loss in human medial vestibular nucleus. Anat Rec 251:431-438.
3. Alvarez JC, Diaz C, Suarez C, Fernandez JA, Gonzalez del Rey C, Navarro A, Tolivia J. 2000. Aging and the human vestibular nuclei: morphometric analysis. Mech Ageing Dev 114:149-172.
4. Arai R, Winsky L, Arai M, Jacobowitz DM. 1991. Immunohistochemical localization of calretinin in the rat hindbrain. J Comp Neurol 310:21-44.
5. Ashley MJ, Gryfe CI, Amies A. 1977. A longitudinal study of falls in an elderly population II. Some circumstances of falling. Age Ageing 6:211-220.
6. Bailey A, Luthert P, Dean A, Harding B, Janota I, Montgomery M, Rutter M, Lantos P. 1998. A clinicopathological study of autism. Brain 121(Pt 5):889-905.
7. Baimbridge KG, Celio MR, Rogers JH. 1992. Calcium-binding proteins in the nervous system. Trends Neurosci 15:303-308.
8. Baizer J, Baker J. 2005a. Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat. Exp Brain Res 164:78-91.
9. Baizer JS, Baker JF. 2005b. Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat. Exp Brain Res 164:78-91.
10. Baizer JS, Baker JF. 2006a. Immunoreactivity for calretinin and calbindin in the vestibular nuclear complex of the monkey. Exp Brain Res 172:103-113.
11. Baizer JS, Baker JF. 2006b. Neurochemically defined cell columns in the nucleus prepositus hypoglossi of the cat and monkey. Brain Res 1094:127-137.
12. Baizer J, Lima R, Witelson SF, Kigar DL, Baker JF. 2006. Immunoreactivity for calretinin defines a subdivision of the medial vestibular nucleus in the human. Neurosci Abs 550.510.
13. Baizer J, Lima R, Witelson S, Kigar D, Baker J. 2007. Neurochemical organization of the inferior olive. Neural Control of Movement Annual Meeting, #83 Seville, Spain.
14. Baker J, Baizer J. 2000. Prolonged horizontal rotation induces c-fos expression in the vestibular nuclear complex of the cat. Neurol Sci Abs 28.
15. Bankoul S, Neuhuber WL. 1992. A direct projection from the medial vestibular nucleus to the cervical spinal dorsal horn of the rat, as demonstrated by anterograde and retrograde tracing. Anat Embryol (Berl) 185:77-85.
16. Barmack NH. 2003. Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res Bull 60:511-541.
17. Barmack NH, Baughman RW, Eckenstein FP, Shojaku H. 1992. Secondary vestibular cholinergic projection to the cerebellum of rabbit and rat as revealed by choline acetyltransferase immunohistochemistry, retrograde and orthograde tracers. J Comp Neurol 317:250-270.
18. Belknap DB, McCrea RA. 1988. Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:13-28.
19. Bergquist F, Ludwig M, Dutia MB. 2008. Role of the commissural inhibitory system in vestibular compensation in the rat. J Physiol 586(Pt 18):4441- 4452.
20. Berman A. 1968. The brain stem of the cat. Madison: University of Wisconsin Press.
21. Blaszczyk JW, Prince F, Raiche M, Hebert R. 2000. Effect of ageing and vision on limb load asymmetry during quiet stance. J Biomech 33:1243-1248.
22. Bloem BR, Steijns JA, Smits-Engelsman BC. 2003. An update on falls. Curr Opin Neurol 16:15-26.
23. Braak H, Rub U, Del Tredici K. 2003. Involvement of precerebellar nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 29:60-76.
24. Brodal A. 1952. Experimental demonstration of cerebellar connexions from the perihypoglossal nuclei (nucleus intercalatus, nucleus praepositus hypoglossal and nucleus of roller) in the cat. J Anat 86:110-129.
25. Brodal A. 1962. The vestibular nuclei and their connections, anatomy and functional correlations. Edinburgh: Oliver and Boyd.
26. Brodal A. 1983. The perihypoglossal nuclei in the macaque monkey and the chimpanzee. J Comp Neurol 218:257-269.
27. Brodal A. 1984. The vestibular nuclei in the macaque monkey. J Comp Neurol 227:252-266.
28. Brodal A, Brodal P. 1983. Observations on the projection from the perihypoglossal nuclei onto the cerebellum in the macaque monkey. Arch Ital Biol 121:151-166.
29. Brodal A, Pompeiano O. 1957. The vestibular nuclei in the cat. J Anat 91:438-454.
30. Broussard DM, Kassardjian CD. 2004. Learning in a simple motor system. Learn Mem (Cold Spring Harbor, NY) 11:127-136.
31. Broussard DM, Lisberger SG. 1992. Vestibular inputs to brain stem neurons that participate in motor learning in the primate vestibuloocular reflex. J Neurophysiol 68:1906-1909.
32. Büttner-Ennever JA. 1992. Patterns of connectivity in the vestibular nuclei. Ann N Y Acad Sci 656:363-378.
33. Büttner-Ennever J, Büttner U. 1988. The reticular formation. In: Büttner-Ennever J, editor. Neuroanatomy of the oculomotor system. Amsterdam: Elsevier. p 119-176.
34. Büttner-Ennever J, Gerrits N. 2004. Vestibular system. In: Paxinos G, Mai JK, editors. The human nervous system. Amsterdam: Elsevier. p 1213-1241.
35. Carleton SC, Carpenter MB. 1984. Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey. Brain Res 294:281-298.
36. Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
37. Cheron G. 1990. Effect of incisions in the brainstem commissural network on the short-term vestibulo-ocular adaptation of the cat. J Vestib Res 1:223-239.
38. Cheron G, Gillis P, Godaux E. 1986a. Lesions in the cat prepositus complex: effects on the optokinetic system. J Physiol 372:95-111.
39. Cheron G, Godaux E, Laune JM, Vanderkelen B. 1986b. Lesions in the cat prepositus complex: effects on the vestibulo-ocular reflex and saccades. J Physiol 372:75-94.
40. D'Angelo E, Rossi P, Armano S, Taglietti V. 1999. Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fiber-granule cell transmission in rat cerebellum. J Neurophysiol 81:277-287.
41. Deckel AW. 1995. Is Huntington's disease of cerebellar/ brainstem origin? Lancet 345:263-264.
42. Epema AH, Gerrits NM, Voogd J. 1988. Commissural and intrinsic connections of the vestibular nuclei in the rabbit: a retrograde labeling study. Exp Brain Res 71:129-146.
43. Essick C. 1912. The development of the nuclei pontis and the nucleus arcuatus in man. Am J Anat 121:25-54.
44. Farrow K, Broussard DM. 2003. Commissural inputs to secondary vestibular neurons in alert cats after canal plugs. J Neurophysiol 89:3351-3353.
45. Gerrits N. 1990. Vestibular nuclear complex. The human nervous system. Philadelphia: Academic Press. p 863-888.
46. Gerrits NM, Voogd J. 1986. The nucleus reticularis tegmenti pontis and the adjacent rostral paramedian reticular formation: differential projections to the cerebellum and the caudal brain stem. Exp Brain Res 62:29-45.
47. Gerrits NM, Voogd J, Nas WS. 1985. Cerebellar and olivary projections of the external and rostral internal cuneate nuclei in the cat. Exp Brain Res 57:239-255.
48. Hendricksen M, Thomas AJ, Ferrier IN, Ince P, O'Brien JT. 2004. Neuropathological study of the dorsal raphe nuclei in late-life depression and Alzheimer's disease with and without depression. Am J Psychiatry 161:1096-1102.
49. Hof PR, Morrison JH. 1990. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: II. Primary and secondary visual cortex. J Comp Neurol 301:55-64.
50. Hof PR, Cox K, Morrison JH. 1990. Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: I. Superior frontal and inferior temporal cortex. J Comp Neurol 301:44-54.
51. Hof PR, Nimchinsky EA, Celio MR, Bouras C, Morrison JH. 1993. Calretinin-immunoreactive neocortical interneurons are unaffected in Alzheimer's disease. Neurosci Lett 152:145-148.
52. Holstein GR, Martinelli GP, Wearne S, Cohen B. 1999. Ultrastructure of vestibular commissural neurons related to velocity storage in the monkey. Neuroscience 93:155-170.
53. Horn AK, Büttner-Ennever JA. 1998. Premotor neurons for vertical eye movements in the rostral mesencephalon of monkey and human: histologic identification by parvalbumin immunostaining. J Comp Neurol 392:413-427.
54. Horn AK, Büttner-Ennever JA, Suzuki Y, Henn V. 1995. Histological identification of premotor neurons for horizontal saccades in monkey and man by parvalbumin immunostaining. J Comp Neurol 359:350-363.
55. Ito M. 2002. The molecular organization of cerebellar long-term depression. Nat Rev Neurosci 3:896-902.
56. Kalchthaler T, Bascon RA, Quintos V. 1978. Falls in the institutionalized elderly. J Am Geriatr Soc 26:424-428.
57. Kevetter GA. 1996. Pattern of selected calcium-binding proteins in the vestibular nuclear complex of two rodent species. J Comp Neurol 365:575-584.
58. Kevetter GA, Leonard RB. 1997. Use of calcium-binding proteins to map inputs in vestibular nuclei of the gerbil. J Comp Neurol 386:317-327.
59. Kevetter GA, Leonard RB, Newlands SD, Perachio AA. 2004. Central distribution of vestibular afferents that innervate the anterior or lateral semicircular canal in the Mongolian gerbil. J Vestib Res 14:1-15.
60. Korte GE. 1979. The brainstem projection of the vestibular nerve in the cat. J Comp Neurol 184:279-292.
61. Koutcherov Y, Huang XF, Halliday G, Paxinos G. 2004. Organization of human brainstem nuclei. In: Paxinos G, Mai JK, editors. The human nervous system. Amsterdam: Elsevier. p 273-321.
62. Kruger L, Saporta S, Swanson LW. 1995. Photographic atlas of the rat brain: the cell and fiber architecture illustrated in three planes with stereotaxic coordinates. Cambridge, MA, New York: Cambridge University Press.
63. LaBossiere E, Glickstein M. 1976. Histological processing for the neural sciences. Springfield, IL: Charles C. Thomas.
64. Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG. 1985a. Floccular efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase. J Comp Neurol 235:26-37.
65. Langer T, Fuchs AF, Scudder CA, Chubb MC. 1985b. Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 235:1-25.
66. Langer T, Kaneko CR, Scudder CA, Fuchs AF. 1986. Afferents to the abducens nucleus in the monkey and cat. J Comp Neurol 245:379-400.
67. Liu S, Wang J, Zhu D, Fu Y, Lukowiak K, Lu YM. 2003. Generation of functional inhibitory neurons in the adult rat hippocampus. J Neurosci 23:732-736.
68. Masui T, Hasegawa Y, Matsuyama Y, Sakano S, Kawasaki M, Suzuki S. 2005. Gender differences in platform measures of balance in rural community-dwelling elders. Arch Gerontol Geriatr 41:201-209.
69. McCrea RA, Horn AK. 2005. Nucleus prepositus. Prog Brain Res 151:205-230.
70. McCrea RA, Baker R, Delgado-Garcia J. 1979. Afferent and efferent organization of the prepositus hypoglossi nucleus. Prog Brain Res 50:653-665.
71. McFarland JL, Fuchs AF. 1992. Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. J Neurophysiol 68:319-332.
72. McGibbon CA. 2003. Toward a better understanding of gait changes with age and disablement: neuromuscular adaptation. Exerc Sports Sci Rev 31:102-108.
73. Milosevic A, Zecevic N. 1998. Developmental changes in human cerebellum: expression of intracellular calcium receptors, calcium-binding proteins, and phosphorylated and nonphosphorylated neurofilament protein. J Comp Neurol 396:442-460.
74. Moreno-Lopez B, Estrada C, Escudero M. 1998. Mechanisms of action and targets of nitric oxide in the oculomotor system. J Neurosci 18:10672-10679.
75. Moreno-López B, Escudero M, De Vente J, Estrada C. 2001. Morphological identification of nitric oxide sources and targets in the cat oculomotor system. J Comp Neurol 435:311-324.
76. Murakawa R, Kosaka T. 1999. Diversity of the calretinin immunoreactivity in the dentate gyrus of gerbils, hamsters, guinea pigs, and laboratory shrews. J Comp Neurol 411:413-430.
77. Ogasawara H, Doi T, Doya K, Kawato M. 2007. Nitric oxide regulates input specificity of long-term depression and context dependence of cerebellar learning. PLoS Comput Biol 3:e179.
78. Olszewski J, Baxter D. 1982. Cytoarchitecture of the human brain stem. Basel: S. Karger.
79. Paxinos G, Huang XF. 1995. Atlas of the human brainstem. San Diego: Academic Press.
80. Paxinos G, Watson C. 1997. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
81. Paxinos G, Carrive P, Wang H, Wang P-Y. 1999. Chemoarchitectonic atlas of the rat brainstem. San Diego: Academic Press.
82. Paxinos G, Huang XF, Toga AW. 2000. The rhesus monkey brain in stereotaxic coordinates. San Diego: Academic Press. 163 [164] of plates p.
83. Peterson BW, Coulter JD. 1977. A new long spinal projection from the vestibular nuclei in the cat. Brain Res 122:351-356.
84. Pimenta AF, Strick PL, Levitt P. 2001. Novel proteoglycan epitope expressed in functionally discrete patterns in primate cortical and subcortical regions. J Comp Neurol 430:369-388.
85. Pompeiano O, d'Ascanio P, Centini C, Pompeiano M, Balaban E. 2002. Gene expression in rat vestibular and reticular structures during and after space flight. Neuroscience 114:135-155.
86. Precht W, Shimazu H, Markham CH. 1966. A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J Neurophysiol 29:996-1010.
87. Résibois A, Rogers JH. 1992. Calretinin in rat brain: an immunohistochemical study. Neuroscience 46:101-134.
88. Romero DH, Stelmach GE. 2003. Changes in postural control with aging and Parkinson's disease. IEEE Eng Med Biol Mag 22:27-31.
89. Roste GK. 1989. Observations on the projection from the perihypoglossal nuclei to the cerebellar cortex and nuclei in the cat. A retrograde WGA-HRP and fluorescent tracer study. Anat Embryol (Berl) 180:521-533.
90. Rüb U, Del Tredici K, Schultz C, Büttner-Ennever JA, Braak H. 2001. The premotor region essential for rapid vertical eye movements shows early involvement in Alzheimer's disease-related cytoskeletal pathology. Vision Res 41:2149-2156.
91. Sadjadpour K, Brodal A. 1968. The vestibular nuclei in man. A morphological study in the light of experimental findings in the cat. J Hirnforsch 10:299-323.
92. Sans N, Moniot B, Raymond J. 1995. Distribution of calretinin mRNA in the vestibular nuclei of rat and guinea pig and the effects of unilateral labyrinthectomy: a non-radioactive in situ hybridization study. Brain Res Mol Brain Res 28:1-11.
93. Sato Y, Kanda K, Ikarashi K, Kawasaki T. 1989. Differential mossy fiber projections to the dorsal and ventral uvula in the cat. J Comp Neurol 279:149-164.
94. Shaw MD, Baker R. 1983. Direct projections from vestibular nuclei to facial nucleus in cats. J Neurophysiol 50:1265-1280.
95. Sherwood CC. 2005. Comparative anatomy of the facial motor nucleus in mammals, with an analysis of neuron numbers in primates. Anat Rec A Discov Mol Cell Evol Biol 287:1067-1079.
96. Sherwood CC, Hof PR, Holloway RL, Semendeferi K, Gannon PJ, Frahm HD, Zilles K. 2005. Evolution of the brainstem orofacial motor system in primates: a comparative study of trigeminal, facial, and hypoglossal nuclei. J Hum Evol 48:45-84.
97. Shin JH, Linden DJ. 2005. An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol 94:4281-4289.
98. Shinder ME, Purcell IM, Kaufman GD, Perachio AA. 2001. Vestibular efferent neurons project to the flocculus. Brain Res 889: 288-294.
99. Slowinski J, Imamura A, Uitti RJ, Pooley RA, Strongosky AJ, Dickson DW, Broderick DF, Wszolek ZK. 2008. MR imaging of brainstem atrophy in progressive supranuclear palsy. J Neurol 255:37-44.
100. Somana R, Walberg F. 1980. A re-examination of the cerebellar projections from the gracile, main and external cuneate nuclei in the cat. Brain Res 186:33-42.
101. Steele JC, Richardson JC, Olszewski J. 1964. Progressive supranuclear palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol 10:333-359.
102. Stein B, Carpenter M. 1967. Central projections of portions of the vestibular ganglia innervating specific part of the labyrinth in the rhesus monkey. Am J Anat 120:281-318.
103. Suarez C, Diaz C, Tolivia J, Alvarez JC, Gonzalez del Rey C, Navarro A. 1997. Morphometric analysis of the human vestibular nuclei. Anat Rec 247:271-288.
104. Ugolini G, Klam F, Doldan Dans M, Dubayle D, Brandi AM, Büttner-Ennever J, Graf W. 2006. Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: differences in monosynaptic input to "slow" and "fast" abducens motoneurons. J Comp Neurol 498:762-785.
105. Walberg F. 1951. The lateral reticular nucleus of the medulla oblongata. A comparative-anatomical study. Acta Psychiatr Neurol Scand Suppl No. 74:92-94.
106. Witelson SF, McCulloch PB. 1991. Premortem and postmortem measurement to study structure with function: a human brain collection. Schizophr Bull 17:583-591.
107. Yu MC, Cho E, Luo CB, Li WW, Shen WZ, Yew DT. 1996. Immunohistochemical studies of GABA and parvalbumin in the developing human cerebellum. Neuroscience 70:267-276.