Reinnervation of the rat olfactory bulb after methyl bromide-induced lesion: Timing and extent of reinnervation

Journal of Comparative Neurology

Volumn 412, Issue 3, 1999, Pages 439-457

  Schwob, James E ^a   Youngentob, Steven L ^a,b   Ring, George ^a   Iwema, Carrie L ^a   Mezza, Renee C ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Axonal guidance; GAP 43; Gliosis; Glomerulotopy; Olfactory marker protein; Regeneration

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; HORSERADISH PEROXIDASE; METHYL BROMIDE; NEUROMODULIN; WHEAT GERM AGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENERVATION; DIET RESTRICTION; GLIOSIS; MALE; NERVE FIBER DEGENERATION; NERVE FIBER TRANSPORT; NERVE LESION; NERVE PROJECTION; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY NERVE; PRIORITY JOURNAL; RAT; REINNERVATION;

ANIMALS; HYDROCARBONS, BROMINATED; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; NERVE DEGENERATION; NERVE REGENERATION; NEUROGLIA; OLFACTORY BULB; OLFACTORY MUCOSA; OLFACTORY NERVE; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 0033610227     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990927)412:3<439::AID-CNE5>3.0.CO;2-H     Document Type: Article

References (79)

1. Bailey MS, Shipley MT. 1993. Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501-526.
2. Baker H, Kawano T, Margolis FL, Joh TH. 1983. Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69-78.
3. Baker H, Kawano T, Albert V, Joh TH, Reis DJ, Margolis FL. 1984. Olfactory bulb dopamine neurons survive deafferentation-induced loss of tyrosine hydroxylase. Neuroscience 11:605-615.
4. Baker H, Towle AC, Margolis FL. 1988. Differential afferent regulation of dopaminergic and GABAergic neurons in the mouse main olfactory bulb. Brain Res 450:69-80.
5. Barber PC, Dahl D. 1987. Glial fibrillary acidic protein (GFAP)-like immunoreactivity in normal and transected rat olfactory nerve. Exp Brain Res 65:681-685.
6. Barber PC, Lindsay RM. 1982. Schwann cells of the olfactory nerves contain glial fibrillary acidic protein and resemble astrocytes. Neuroscience 7:3077-3090.
7. Burd GD. 1993. Morphological study of the effects of intranasal zinc sulfate irrigation on the mouse olfactory epithelium and olfactory bulb. Microsc Res Tech 24:195-213.
8. Carr VM, Murphy SP, Morimoto RI, Farbman AI. 1994. Small subclass of rat olfactory neurons with specific bulbar projections is reactive with monoclonal antibodies to the HSP70 heat shock protein. J Comp Neurol 348:150-160.
9. Carr VMcM, Ring G, Youngentob SL, Schwob JE, Farbman AI. 1998. HSP70 (+) olfactory receptor neuron (ORN) bulbar projections following methyl bromide (MeBr) lesion of the rat olfactory epithelium (OE). Soc Neurosci Abstr 24:1144.
10. Chiu K, Greer CA 1996. Immunocytochemical analyses of astrocyte development in the olfactory bulb. Dev Brain Res 95:28-37.
11. Chuah MI, Tennent R, Jacobs I. 1995. Response of olfactory Schwann cells to intranasal zinc sulfate irrigation. J Neurosci Res 42:470-478.
12. Costanzo RM. 1991. Regeneration of olfactory receptor cells. Ciba Found Symp 160:233-242.
13. Costanzo RM. 1997. Do odor maps change after recovery from olfactory nerve transection? Chem Senses 22:664.
14. Covault J, Sanes JR. 1986. Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J Cell Biol 102:716-730.
15. Doty RL. 1979 A review of olfactory dysfunction in man. Am J Otolaryngol 101:57-79.
16. Doucette R. 1984. The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat Rec 210:385-391.
17. Doucette R. 1993. Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Micro Res Tech 24:113-130.
18. Esiri MM, Wilcock GK 1984. The olfactory bulbs in Alzheimer's disease. J Neurol Neurosurg Psychiatry 47:56-60.
19. Farbman AI. 1990. Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci 13:362-365.
20. Graziadei PPC, Monti Graziadei GA. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1-18.
21. Graziadei PPC, Monti Graziadei GA. 1980. Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J Neurocytol 9:145-162.
22. Graziadei PPC, Monti Graziadei GA. 1985. Neurogenesis and plasticity of the olfactory sensory neurons. Ann N Y Acad Sci 457:127-142.
23. Halasz N, Greer CA. 1993. Terminal arborizations of olfactory nerve fibers in the glomeruli of the olfactory bulb. J Comp Neurol 337:307-316.
24. Harding J, Graziadei PPC, Monti Graziadei GA, Margolis FL. 1977. Denervation in the primary olfactory pathway of mice. IV. Biochemical and morphological evidence for neuronal replacement following nerve section. Brain Res 132:11-28.
25. 4 irrigation on behavior biochemistry and morphology. Brain Res 140:271-285.
26. Hastings L, Miller ML, Minnema DJ, Evans J, Radike M. 1991. Effects of methyl bromide on the rat olfactory system. Chem Senses 16:43-55.
27. Huard JMT, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE. 1998. Olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neuronal cells. J Comp Neurol 400:469-486.
28. Hurtt ME, Morgan KT, Working PK. 1987. Histopathology of acute toxic responses in selected tissues from rats exposed by inhalation to methyl bromide. Fundam Appl Toxicol 9:352-365.
29. Hurtt ME, Thomas DA, Working PK, Monticello TM, Morgan KT. 1988. Degeneration and regeneration of the olfactory epithelium following inhalation exposure to methyl bromide: pathology cell kinetics and olfactory function. Toxicol Appl Pharmacol 94:311-328.
30. Iwema CL, Youngentob SL, Breer HL, Schwob JE. 1997. Distribution of POR-defined neuronal subtypes in the olfactory epithelium following recovery from peripheral lesion. Soc Neurosci Abstr 23:738.
31. Jafek BW, Hartman D, Eller PM, Johnson EW, Strahan RC, Moran DT. 1990. Postviral olfactory dysfunction. Am J Rhinol 4:91-100.
32. Kawano T, Margolis FL. 1982. Transsynaptic regulation of olfactory bulb catecholamines in mice and rats. J Neurochem 39:342-348.
33. Koster NL, Costanzo RM. 1996. Electrophysiological characterization of the olfactory bulb during recovery from sensory deafferentation. Brain Res 724:17-20.
34. Kream RM, Margolis FL. 1984 Olfactory marker protein: turnover and transport in normal and regenerating neurons. J Neurosci 4:868-879.
35. Mackay-Sim A, Kittel P. 1991. Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J Neurosci 11:979-984.
36. Margolis FL. 1974. Carnosine in the primary olfactory pathway. Science 184:909-911.
37. 4 and its subsequent regeneration. Am J Anat 142:67-90.
38. Matulionis DH. 1976. Light and electron microscopic study of the degeneration and early regeneration of olfactory epithelium in the mouse. Am J Anat 145:79-100.
39. Meiri KF, Bickerstaff LE, Schwob JE. 1991. Monoclonal antibodies show that kinase C phosphorylation of GAP-43 during axonogenesis is both spatially and temporally restricted in vivo. J Cell Biol. 112:991-1005.
40. Mesulam M-M, Hegarty E, Barbas H, Carson KA, Gower EC, Knapp AG, Moss MB, Mufson EJ. 1980. Additional factors influencing sensitivity in the tetramethyl benzidine method for horseradish peroxidase neurohistochemistry. J Histochem Cytochem 28:1255-1259.
41. Mombaerts P, Wang F, Dulac F, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
42. Monti Graziadei GA, Graziadei PPC. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol 8:197-213.
43. Monti Graziadei GA, Margolis FL, Harding JW, Graziadei PPC. 1977. Immunocytochemistry of the olfactory marker protein. J Histochem Cytochem 25:1311-1316.
44. Monti Graziadei GA, Karlan MS, Bernstein JJ, Graziadei PPC. 1980. Reinnervation of the olfactory bulb after section of the olfactory nerve in monkey, Saimiri sciureus. Brain Res 189:343-354.
45. Morrison EE, Costanzo RM. 1995. Regeneration of olfactory sensory neurons and reconnection in the aging hamster central nervous system. Neurosci Lett 198:213-217.
46. Mulvaney BD, Heist HE. 1971. Regeneration of rabbit olfactory epithelium. Am J Anat 131:241-252.
47. Nadi NS, Head R, Grillo M, Hempstead J, Grannot-Reisfeld N, Margolis FL. 1981. Chemical deafferentation of the olfactory bulb: plasticity of the levels of tyrosine hydroxylase dopamine and norepinephrine. Brain Res 213:365-377.
48. Nagahara Y. 1940. Experimentelle Studien uber die histologischen Veranderungen des Geruchsorgans nach der Olfactoriusdurschschneidung Beitrage zur Kenntnis des feinereer Baus der Geruchsorgan. Jpn J Med Sci 5:165-199.
49. Pinching AJ, Powell TPS. 1971. The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347-377.
50. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
51. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 74:1245-1255.
52. Ring G, Youngentob SL, Schwob JE. 1995. Identification of a discrete subset of rat olfactory glomeruli and their reinnervation following methyl bromide lesion. Chem Senses 20:765.
53. Ring GD, Mezza RC, Schwob JE. 1997. Identification of discrete subsets of rat olfactory glomeruli and neurons. J Comp Neurol 388:415-434.
54. Schoenfeld TA, Clancy AN, Forbes WB, Macrides F. 1994. The spatial organization of the peripheral olfactory system of the hamster. Part I: Receptor neuron projections to the main olfactory bulb. Brain Res Bull 34:183-210.
55. Schwob JE, Gottlieb DI. 1986. The primary olfactory projection has two chemically distinct zones. J Neurosci 6:3393-3404.
56. Schwob JE, Youngentob SL. 1991. Reconstitution of the olfactory epithelium and reinnervation of the olfactory bulb after methyl bromide lesions. Soc Neurosci Abstr 17:635.
57. Schwob JE, Youngentob SL. 1992. Reconstitution of the olfactory epithelium and reinnervation of the olfactory bulb after methyl bromide lesions. Chem Senses 17:696.
58. Schwob JE, Mieleszko Szumowski KE, Stasky AA. 1992. Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J Neurosci 12:3896-3919.
59. Schwob JE, Hershberger JM, Youngentob. 1993. Reinnervation of the olfactory bulb after epithelial lesion. Soc Neurosci Abstr 19:12.
60. Schwob JE, Youngentob SL, Meiri KF. 1994. On the formation of neuromata in the peripheral olfactory system. J Comp Neurol 340:361-380.
61. Schwob JE, Youngentob SL, Mezza RC. 1995. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J Comp Neurol 359:15-37.
62. Shipley MT. 1985. Transport of molecules from nose to brain: transneuronal anterograde and retrograde labeling in the rat olfactory system by wheat germ agglutinin-horseradish peroxidase applied to the nasal epithelium. Brain Res Bull 15:129-142.
63. Singer MS, Shepherd GM, Greer CA. 1995. Olfactory receptors guide axons. Nature 377:19-20.
64. Smith CG. 1938. Pathologic change in olfactory nasal mucosa of albino rats with "stunted" olfactory bulbs. Arch Otolaryngol 31:131-143.
65. Smith RL, Baker H, Kolstad K, Spencer DD, Greer CA. 1991. Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulb. Brain Res 548:140-148.
66. Strotmann J, Wanner I, Krieger J, Raming K, Breer H. 1992. Expression of odorant receptors in spatially restricted subsets of chemosensory neurones. Neuroreport 3:1053-1056.
67. Strotmann J, Wanner I, Helfrich T, Beck A, Breer H. 1994. Rostrocaudal patterning of receptor-expressing neurons in the rat nasal cavity. Cell Tissue Res 278:11-20.
68. Valverde F, Lopez-Mascaraque L. 1991. Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J Comp Neurol 307:658-674.
69. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
70. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
71. Verhaagen J, Oestreicher AB, Gispen WH, Margolis FL. 1989. The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J Neurosci 9:683-691.
72. Verhaagen J, Oestreicher AB, Grillo M, Khew-Goodall Y-S, Gispen WH, Margolis FL. 1990. Neuroplasticity in the olfactory system: differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. J Neurosci Res 26:31-44.
73. Walters E, Buchheit K, Maruniak JA. 1992. Receptor neuron losses result in decreased cytochrome P-450 immunoreactivity in associated non-neuronal cells of mouse olfactory mucosa. J Neurosci Res 33:103-111.
74. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
75. Yee KK, Costanzo RM. 1995. Restoration of olfactory mediated behavior after olfactory bulb deafferentation. Physiol Behav 58:959-968.
76. Youngentob SL, Schwob JE. 1991. Olfactory function after peripheral olfactory lesions. Soc Neurosci Abstr 17:635.
77. Youngentob SL, Schwob JE. 1992. Recovery of odorant identification following methyl bromide induced lesions of the olfactory epithelium. Chem Senses 17:726.
78. Youngentob SL, Schwob JE. 1997. Changes in odorant quality perception following methyl bromide induced lesions of the olfactory epithelium. Chem Senses 22:830-831.
79. Youngentob SL, Schwob JE, Sheehe PR, Markert LM. 1997. Odorant threshold following methyl bromide-induced lesions of the olfactory epithelium. Physiol Behav 62:1241-1252.