Morphological evidence for local microcircuits in rat vestibular maculae

Journal of Comparative Neurology

Volumn 379, Issue 3, 1997, Pages 333-346

  Ross, Muriel D ^a  

^a NASA AMES RESEARCH CENTER   (United States)

Author keywords

3 D reconstruction; C synapse; calyx; efferents; hair cells

Indexed keywords

ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; CELL TYPE; HAIR CELL; INFORMATION PROCESSING; MALE; NONHUMAN; NONMYELINATED NERVE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPSE; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; VESTIBULAR LABYRINTH;

NASA CENTER ARC; NASA DISCIPLINE NEUROSCIENCE;

ACOUSTIC MACULAE; ANIMALS; EAR, INNER; MALE; MICROSCOPY, ELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; VESTIBULAR NUCLEI;

EID: 0031043836     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970317)379:3<333::AID-CNE2>3.0.CO;2-4     Document Type: Article

References (81)

1. Abou-Madi, L., P. Pontarotti, G. Tramu, A. Cupo, and M. Eybalin (1987) Coexistence of putative neuroactive substances in lateral olivocochlear neurons of rat and guinea pig. Hearing Res. 30:135-146.
2. Ades, H.W., and H. Engström (1965) Form and innervation of the vestibular epithelia. In A. Graybiel (ed): The Role of the Vestibular Organs in the Exploration of Space. Washington, DC: NASA, pp. 23-41.
3. Altschuler, R.A., J. Fex, M.H. Parakkal, and F. Eckenstein (1984) Colocalization of enkephalin-like and choline acetyltransferase-like immunoreactivities in olivocochlear neurons of the guinea pig. J. Histochem. Cytochem. 32:839-843.
4. American Veterinary Medical Association (1993) Report of the AVMA Panel on Euthanasia. J. Am. Vet. Med. Assoc. 202:229-249.
5. Bagger-Sjöback, D., and R.L. Gulley (1979) Synaptic structures in the type II hair cell in the vestibular system of the guinea pig. Acta Otolaryngol. (Stockh.) 88:401-411.
6. Bartfai, T., K. Iverfeldt, E. Brodin, and S.-O. Ögren (1986) Functional consequences of coexistence of classical and peptide neurotransmitters. Brain Res. 68:321-330.
7. Bernander, O., R.J. Douglas, K.A.C. Martin, and C. Koch (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Nat. Acad. Sci. U.S.A. 88:11569-11573.
8. Birks, R.I., H.E. Huxley, and B. Katz (1974) The fine structure of the neuromuscular junction of the frog. J. Physiol. (Lond.) 150:134-344.
9. Black, I.B., J.E. Adler, C.F. Dreyfus, W.F. Friedman, E.F. LaGamma, and A.H. Roach (1987) Biochemistry of information storage in the nervous system. Science 236:1263-1268.
10. Bodian, D. (1966) Synaptic types on spinal motoneurons: an electron microscope study. Bull. Johns Hopkins Hosp. 119:16-45.
11. Carpenter, M.B., L. Chang, A.B. Perira, L.B. Hersh, G. Bruce, and J.Y. Wu (1987) Vestibular and cochlear efferent neurons in the monkey identified by immunocytochemical methods. Brain Res. 408:275-280.
12. Chimento, T.C., and M.D. Ross (1996) Evidence for a sensory processing unit in the vestibular macula. In S.M. Highstein, B. Cohen and J.A. Buttner-Ennever (eds): New Directions in Vestibular Research. New York: Ann. N.Y. Acad. Sci., vol. 781 pp. 196-212.
13. Chimento, T.C., D.G. Doshay, and M.D. Ross (1994) Compartmental modeling of rat macular primary afferents from three-dimensional reconstructions of transmission electron micrographs of serial sections. J. Neurophysiol. 71:1883-1896.
14. Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9:268-287.
15. Connaughton, M., J.V. Priestley, M.V. Sofroniew, F. Eckenstein, and A.C. Cuello (1986) Electron microscopic immunocytochemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies. Neuroscience 17:205-224.
16. Conradi, S. (1969) Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiol. Scand. 332:85-111.
17. Desmond, J.L., and W.B. Levy (1988) Anatomy of associative long-term synaptic modification. Neurol. Neurobiol. 35:201-264.
18. Didier, A., J. Dupont, and Y. Cazals (1990) GABA immunoreactivity of calyceal nerve endings in the vestibular system of the guinea pig. Cell Tissue Res. 260:415-419.
19. Douglas, R.J., and K.A.C. Martin (1991) Opening the grey box. TIN 14:286-293.
20. Engström, H. (1958) On the double innervation of the sensory epithelia of the inner ear. Acta Otolaryngol. (Stockh.) 49:109-118.
21. Engström, H., H. Lindeman, and H.W. Ades (1966) Anatomical features of the auricular sensory organs. In J. Huertas and A. Graybiel (eds): Second Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: NASA, pp. 33-54.
22. Fex, J. (1967) Efferent inhibition in the cochlea related to hair-cell dc activity: study of postsynaptic activity of the crossed olivo-cochlear fibers in the cat. J. Acoust. Soc. Am. 41:666-675.
23. Foster, J.D., M.J. Drescher, and D.G. Drescher (1995) Immunohistochemical localization of GABA receptors in the mammalian crista ampullaris. Hear. Res. 83:203-208.
24. Fried, G., L. Terenius, T. Hökfelt, and M. Goldstein (1985) Evidence for differential localization of noradrenaline and neuropeptide Y (NPY) in neuronal storage vesicles isolated from vas deferens. J. Neurosci. 5:450-458.
25. Fuchs, P.A., and B.W. Murrow (1992) Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J. Neurosci. 12:800-809.
26. Fujimoto, S., K. Yamamoto, K. Kuba, K. Morita, and E. Kato (1980) Calcium localization in the sympathetic ganglion of the bullfrog and effects of caffeine. Brain Res. 202:21-32.
27. Galambos, R. (1960) Studies of the auditory system with implanted electrodes. In G.L. Rasmussen and W.F. Windle (eds): Neural Mechanisms of the Auditory and Vestibular Systems. Springfield, IL: Charles C.Thomas, pp. 137-151.
28. Goldberg, J.M., A. Lysakowski, and C. Fernández (1990) Morphophysiological and ultrastructural studies in the mammalian cristae ampullares. Hear. Res. 49:89-102.
29. Gualtierotti, T, and S.J. Gerathewohl (1965) Spontaneous firing and responses to linear acceleration of single otolith units of the frog during short periods of weightlessness during parabolic flight. In A. Graybiel (ed): The Role of the Vestibular Organs in the Exploration of Space. Pensacola, FL: NASA vol. SP 77, pp. 221-229.
30. Hamilton, D.W. (1968) The calyceal synapse of type I vestibular hair cells. J. Ultrastruct. Res. 23:98-114.
31. Harris, K.M., and J.K. Stevens (1989) Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9:2982-2997.
32. Hilding, D., and J. Wersäll (1962) Cholinesterase and its relation to the nerve endings in the inner ear. Acta Otolaryngol. (Stockh.) 55:205-217.
33. Hökfelt, T., O. Johansson, Å. Ljungdahl, J.M. Lundberg, and M. Schultzberg (1980) Peptidergic neurons. Nature 284:515-521.
34. Hökfelt, T., V.R. Holets, W. Staines, B. Meister, T. Melander, M. Schalling, M. Schultzberg, J. Freedman, H. Björklund, L. Olson, B. Lindh, L.-G. Elfvin, J.M. Lundberg, J.Å. Lindgren, B. Samuelsson, B. Pernou, L. Terenius, C. Post, B. Everitt, and M. Goldstein (1986) Coexistence of neuronal messengers - an overview. In T. Hökfelt, K. Fuxe, and B. Pernow (eds): Progress in Brain Research. Amsterdam: Elsevier Science Publishers B.V., pp. 33-70.
35. Holmes, W.R., and C.D. Woody (1989) Effects of uniform and non-uniform synaptic 'activation-distributions' on the cable properties of modeled cortical pyramidal neurons. Brain Res. 505:12-22.
36. Hosokawa, T., D.A. Rusakov, T.V.P. Bliss, and A. Fine (1995) Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J. Neurosci. 15:5560-5573.
37. Housley, G.D., and J.F. Ashmore (1991) Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc. R. Soc. Lond. (Biol.) 244:161-167.
38. Ichimura, T., and P.H. Hashimoto (1988) Structural components in the synaptic cleft captured by freeze-substitution and deep etching of directly frozen cerebellar cortex. J. Neurocytol. 17:3-12.
39. Iurato, S., and G. Taidelli (1964) Relationships and structure of the so-called 'much granulated nerve endings' in the crista ampullaris (as studied by means of serial sections.) Electron Microscopy: 3rd Eur. Reg. Conf. Prague, B:325-326.
40. Lorente de Nó, R. (1931) Ausgewahlte Kapitel aus der vergleichenden Physiologie des Labyrinths. Ergebn. Physiol. 32:73-242.
41. Lundberg, J.M., G. Fried, J. Fahrenkrug, B. Holmstedt, T. Hökfelt, H. Lagercrantz, G. Lundgren, and A. Anggård (1981) Subcellular fractionation of cat submandibular gland: comparative studies on the distribution of actylcholine and vasoactive intestinal polypeptide (VIP). Neuroscience 6:1001-1010.
42. Lysakowski, A., L.B. Minor, C. Ferández, and J.M. Goldberg (1995) Physiological identification of morphologically distinct afferent classes innervating the cristae ampullares of the squirrel monkey. J. Neurophysiol. 73(3):1270-1281.
43. McCue, M.R., and J.J. Guinan (1994) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J. Neurosci. 14:6071-6083.
44. McLaughlin, B.J. (1972) The fine structure of neurons and synapses in the motor nuclei of the cat spinal cord. J. Comp. Neurol. 144:429-460.
45. Montgomery, K., and M.D. Ross (1993) A method for semiautomated serial section reconstruction and visualization of neural tissue from TEM images. In R.J. Ascharya and D.B. Goldgof (eds): Biomedical Image Processing and Biomedical Visualization. Salem, MA: Proc SPIE, pp. 114-120.
46. Montgomery, K., and M.D. Ross (1994) Improvements in semiautomated serial-section reconstruction and visualization of neural tissue from TEM images. Proc. SPIE 2184:264-267.
47. Ohmori, H. (1991) Mechano-electrical transduction in the chicken hair cell. Acta Otolaryngol. Suppl. (Stockh.) 481:1-4.
48. Peters, A., S.L. Palay, and H. deF. Webster (1991) The Fine Structure of the Nervous System: Neurons and Their Supporting Cells, Third Edition. Oxford: Oxford University Press.
49. Pfenninger, K.H. (1971) The cytochemistry of synaptic densities. II. Proteinaceous components and the mechanism of synaptic connectivity. J. Ultrastruct. Res. 35:451-475.
50. Purcell, I.M., and A.A. Perachio (1995) Regional distributions of efferent innervation in the utricular maculae of the gerbil Soc. Neurosci. [Abstr.] 21:399.
51. Rakic, P. (1975) Local circuit neurons. Neurosci. Res. Program Bull. 13:291-446.
52. Raymond, J., D. Dememes, and A. Nieoullon (1988) Neurotransmitters in vestibular pathways. Prog. Brain Res. 76:29-43.
53. Rosenbluth, J. (1962) Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13:405-421.
54. Ross, M.D. (1973) Autonomic components of the VIIIth nerve. Adv. Otorhinolarnygol. 20:316-336.
55. Ross, M.D. (1981) Centrally originating efferent terminals on hair cells: Fact or fancy? In T. Gualtierotti (ed): The Vestibular System: Function and Morphology. New York: Springer-Verlag, pp. 160-183.
56. Ross, M.D. (1985) Anatomic evidence for peripheral neural processing in mammalian graviceptors. Aviat. Space Environ. Med. 56:338-343.
57. Ross, M.D. (1993a) Morphological changes in rat vestibular system following weightlessness. J. Vest. Res. 3:241-251.
58. Ross M.D. (1993b) Ultrastructural evidence of vestibular efferent synapses of intrinsic afferent origin. Soc. Neurosci. [Abstr.] 19:1492.
59. Ross, M.D., C.M. Rogers, and K.M. Donovan (1986) Innervation patterns in rat saccular macula: a structural basis for complex sensory processing. Acta Otolaryngol. (Stockh). 102:75-86.
60. Ross, M.D., L. Cutler, G. Meyer, T. Lam, and P. Vaziri (1990) 3-D components of a biological neural network visualized in computer generated imagery. I. Macular receptive field organization. Acta Otolaryngol. (Stockh). 109:83-92.
61. Ross, M.D., L. Cutler, D. Doshay, R. Cheng, and A. Naddaf (1991) A new theory of macular organization based on computer-assisted 3-D reconstruction, Monte Carlo simulation and symbolic modeling of vestibular maculas. Acta Otolaryngol. Suppl. (Stockh.) 481:11-14.
62. Ross, M.D., T. Chimento, D. Doshay, and R. Cheng (1992) Computer-assisted three-dimensional reconstruction and simulations of vestibular macular neural connectivities. Ann. N.Y. Acad. Sci. 656:75-91.
63. Sans, A., and E. Scarfone (1996) Afferent calyces and type I hair cells during development. A new morphofunctional hypothesis. In S.M. Highstein, B. Cohen and J.A. Buttner-Ennever (eds): New Directions in Vestibular Research. Ann. N.Y. Acad. Sci. 781:1-12.
64. Scarfone, E., D. Dememes, R. Jahn, P. De Camilli, and A. Sans (1988) Secretory function of the vestibular nerve calyx suggested by presence of vesicles, Synapsin 1, and synaptophysin. J. Neurosci. 8:4640-4645.
65. Schmitt, F.O. (1979) The role of structural, electrical and chemical circuitry in brain function. In F.O. Schmitt (ed): The Neurosciences: Fourth Study Program. New York: Rockefeller Univ. Press, pp. 5-20.
66. Schmitt, F.O., P. Dev, and B.H. Smith (1976) Electrotonic processing of information by brain cells. Science 193:114-120.
67. Shepherd, G.M. (1970) The olfactory bulb as a simple cortical system: Experimental analysis and functional implications. In F.O. Schmitt (ed): The Neurosciences: Second Study Program. New York: Rockefeller Univ. Press, pp. 539-552.
68. 2+ concentration in chick cochlear hair cells. J. Physiol. (Lond.). 420:127-148.
69. + channels. J. Physiol. (Lond.) 442:669-690.
70. Smith, C.A., and G.L. Rasmussen (1967) Nerve endings in the maculae and cristae of the chinchilla vestibule, with a special reference to the efferents. In A. Graybiel (ed): Proceedings of Third Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: NASA, SP-152:183-201.
71. Smith, C.A., and F. Sjostrand (1961) A synaptic structure in the hair cells of the guinea pig cochlea. J. Ultrastruct. Res. 5:184-192.
72. Sobkowicz, H.M., S.M. Slapnick, and B.K. August (1993) Presynaptic fibres of spiral neurons and reciprocal synapses in the organ of Corti in culture. J. Neurocytol. 22:979-993.
73. Spoendlin, H. (1965) Ultrastructural studies of the labyrinth in squirrel monkeys. In A. Graybiel (ed): The Role of the Vestibular Organs in the Exploration of Space. Washington, DC: NASA, vol. SP-77, pp. 7-21.
74. Spoendlin, H. (1966) Some morphofunctional and pathological aspects of the vestibular sensory epithelia. In Second Symposium on the Role of the Vestibular Organs in Space Exploration. Washington, DC: NASA, vol. SP-115, pp. 99-115.
75. Usami, S., M. Igarashi, and G.C. Thompson (1987) GABA-like immunoreactivity in the squirrel monkey vestibular endorgans. Brain Res. 417:367-370.
76. Usami, S., J. Hozawa, M. Tazawa, H. Jin, A. Matsubara, and S. Fujita (1991) Localization of substance P-like immunoreactivity in guinea pig vestibular endorgans and the vestibular ganglion. Brain Res. 555:153-158.
77. Viveros, O.H., E.L. Diliberto, E. Hazum, and K.-J. Chang (1979) Opiate-like materials in the adrenal medulla: evidence for storage and secretion with catecholamines. Mol. Pharmacol. 16:1101-1108.
78. Wackym, P.A. (1993) Ultrastructural organization of calcitonin generelated peptide immunoreactive efferent axons and terminals in the vestibular periphery. Am. J. Otol. 14:41-50.
79. Wersäll, J. (1956) Studies on the structure and innervation of the sensory epithelium of the cristae ampullares in the guinea-pig. Acta Otolaryngol. (Suppl.) 126:1.
80. 2+ concentration in vestibular hair cells of the guinea pig. Acta Otolaryngol. Suppl. (Stockh.) 500:26-30.
81. Ylikoski, J., U. Pirvola, O. Happola, P. Panula, and I. Virtanen (1989) Immunohistochemical demonstration of neuroactive substances in the inner ear of rat and guinea pig. Acta Otolaryngol. (Stockh.) 107:417-423.