Intracochlear injection of pseudorabies virus labels descending auditory and monoaminerg projections to olivocochlear cells in guinea pig

European Journal of Neuroscience

Volumn 18, Issue 6, 2003, Pages 1439-1447

  Horváth, Miklós ^a   Ribári, Ottó ^a   Répássy, Gábor ^a   Tóth, Ida E ^a   Boldogkõi, Zsolt ^a   Palkovits, Miklós ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Auditory pathway; Noradrenaline; Olivocochlear system; Serotonin; Transneuronal labelling

Indexed keywords

ACOUSTIC NERVE FIBER; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; BRAIN STEM; CELL LABELING; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; GUINEA PIG; IMMUNOHISTOCHEMISTRY; LOCUS CERULEUS; MALE; MEDIAL GENICULATE BODY; MONOAMINERGIC NERVE; NERVE PROJECTION; NONHUMAN; PONS; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS;

ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; BIOGENIC MONOAMINES; COCHLEA; FUNCTIONAL LATERALITY; GUINEA PIGS; HERPESVIRUS 1, SUID; LOCUS COERULEUS; MALE; NEURONS; OLIVARY NUCLEUS; PSEUDORABIES; RAPHE NUCLEI; TIME FACTORS;

EID: 0141816714     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02870.x     Document Type: Article

References (87)

1. Anderson, R.A., Knight, P.L. & Merzenich, M.M. (1980) The thalamocortical and corticothalamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: evidence for two largely segragated systems of connections. J. Comp. Neurol., 194, 663-701.
2. Appeltants, D., Ball, G.F. & Balthazart, J. (2002) The origin of chatecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport, 13, 649-653.
3. Aschoff, A. & Ostwald, J. (1987) Different origin of cochlear efferents in some bat species, rats and guinea pigs. J. Comp. Neurol., 264, 56-72.
4. Aschoff, A. & Ostwald, J. (1988) Distribution of cochlear efferents and olivo-collicular neurons in the brainstem of rat and guinea pig. Exp. Brain. Res., 71, 241-251.
5. Aston-Jones, G. & Card, J.P. (2000) Use of pseudorabies virus to delineate multisynaptic circuits in brain: opportunities and limitations. J. Neurosci. Meth., 103, 51-61.
6. Bartha, A. (1961) Experiments to reduce the virulance of AujeszkT's disease virus. [In Hungarian.] Magyar Állatorvosok Lapja, 16, 42.
7. Behrens, E.G., Schoefield, B.R. & Thompson, A.M. (2002) Aminergic projections to cochlear nucleus via descending auditory pathways. Brain Res., 955, 34-44.
8. Billig, I., Foris, J., Card, J.P. & Yates, B.J. (1999) Transneuronal tracing of neural pathways controlling an abdominal muscle, rectus abdominus, in the ferret. Brain Res., 820, 31-44.
9. Brideau, A.D., Card, J.P. & Enquist, L.W. (2000) Role of pseudorabies virus Us9, a type II membrane protein, in infection of tissue culture cells and the rat nervous system. J. Virol., 74, 834-845.
10. Büki, B., Wit, H.P. & Avan, P. (2000) Olivocochlear efferent vs. middle-ear contributions to the alteration of otoacoustic emissions by contralateral noise. Brain Res., 852, 140-150.
11. Caicedo, A. & Herbert, H. (1993) Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J. Comp. Neurol., 328, 377-392.
12. Card, J.P., Rinaman, L., Lynn, R.B., Meade, R.P., Miselis, R.R. & Enquist, L.W. (1993) Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport and pathogenesis. J. Neurosci., 13, 2515.
13. Card, J.P., Whealy, M.E., Robbins, A.K. & Enquist, L.W. (1992) Pseudorabies virus envelope glycoprotein gI influences both neurotropism and virulence during infection of the rat visual system. J. Virol., 66, 3032-3041.
14. Chen, S., Ming, X., Miselis, R. & Aston-Jones, G. (1999) Characterization of transsynaptic tracing with central application of Pseudorabies virus. Brain Res., 838, 171-183.
15. Desmedt, J.E. (1975) Physiological studies of the efferent recurrent auditory system. In Keidel, W.D. & Neff, W.D. (eds), Handbook of Sensory Physiology. Springer, Berlin, pp. 219-246.
16. Diamond, I.T., Jones, E.G. & Powell, T.P.S. (1969) The projection of the auditory cortex upon the diencephalon and brainstem in the cat. Brain Res., 15, 305-340.
17. Dobbins, E.G. & Feldman, J.L. (1995) Differential innervation of protruder and retractor muscles of the tongue in rat. J. Comp. Neurol., 357, 376-380.
18. Enquist, L.W., Husak, P.J., Banfield, B.W. & Smith, G.A. (1999) Infection and spread of alpha herpes viruses in the nervous system. Adv. Viral. Res., 51, 237-347.
19. Faye-Lund, H. (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat. Embryol., 175, 35-52.
20. Giraud, A.L., Garnier, S., Micheyl, C., Lina, G., Chays, A. & Chery-Croze, S. (1997) Auditory efferents involved in speech-in-noise intelligibility. Neuroreport, 8, 1779-1783.
21. Guillery, R.W. & Herrup, K. (1997) Quantification without pontification: Choosing a method for counting objects in sectioned tissues. J. Comp. Neurol., 386, 2-7.
22. Guinan, J.J. (1996) Physiology of olivocochlear efferents. In Dallos, P., Popper, A.N. & Fay, R.R. (Eds), The Cochlea. Springer, New York, pp 435-502.
23. Herrera, M., Hurtado-Garcia, J.F., Collia, F. & Lanciego, J. (1994) Projections from the primary auditory cortex onto the dorsal cortex of the inferior colliculus in albino rats. Arch. Ital. Biol., 132, 147-164.
24. Horváth, M., Kraus, K.S. & Illing, R.B. (2000) Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat. J. Comp. Neurol., 422, 95-105.
25. Huffman, R.F. & Henson, O.W. (1990) The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res. Rev., 15, 295-323.
26. Hughes, E.C., Gott, P.S., Weinstein, R.C. & Binggeli, R. (1988) Noradrenergic cerebral stimulation of sensorineural impaired subjects: yohimbine effects on specch intelligibility and the auditory brain response. Am. J. Otol., 9, 122-126.
27. Jansen, A.S.P., Van Nguyen, X., Karpitskiy, V., Mettenleiter, T.C. & Loewy, A.D. (1995) Central command neurons of the sympathetic nervous system: basis of the flight-or-fight response. Science, 270, 253-260.
28. Jasmin, L., Burkey, A.R., Card, J.P. & Basbaum, A. (1997) Transneuronal labelling of a nociceptive pathway, the spino-(trigemino-) parabrachioamygdaloid, in the rat. J. Neurosci., 17, 3751-3765.
29. Kane, E.S. & Conlee, J.W. (1979) Descending inputs to the caudal cochlear nucleus of the cat: degeneration and autoradiographic studies. J. Comp. Neurol., 187, 759-784.
30. Khalfa, S., Bougeard, R., Morand, N., Veuillet, E., Isnard, J., Guenot, M., Fischer, C. & Collet, L. (2001) Evidence of peripheral auditory activity modulation by the auditory cortex in humans. Neuroscience, 104, 347-358.
31. Klepper, A. & Herbert, H. (1991) Distribution and origin of noradrenergic and serotoninergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Res., 557, 190-201.
32. Kuypers, H.G. & Ugolini, G. (1990) Viruses as transneuronal tracers: Trends Neurosci., 13, 71-75.
33. Leak, R.K., Card, J.P. & Moore, L.Y. (1999) Suprachiasmatic pacemaker organization analyzed by transynaptic transport. Brain. Res., 819, 214-224.
34. Li, Y.W., Ding, Z.Q., Wesselingh, S.L. & Blessing, W.W. (1992) Renal and adrenal sympathetic preganglionic neurons in rabbit spinal cord. Brain Res., 573, 147.
35. Loewy, A.D. (1991) Forebrain nuclei involved in autonomic control (Review). Prog. Brain Res., 87, 253-268.
36. Loewy, A.D. (1995) Pseudorabies virus: a transneuronal tracer for neuroanatomical studies. In Kaplitt, M.G. & Loewy, A.D. (eds), Viral Vectors, Gene Therapy and Neuroscience Applications. Academic Press, San Diego, pp. 349-366.
37. Moore, R.Y. & Goldberg, J.M. (1966) Projections of the inferior colliculus in the monkey. Exp. Neurol., 14, 429-438.
38. Mulders, W.H. & Robertson, D. (2000a) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hear. Res., 144, 65-72.
39. Mulders, W.H. & Robertson, D. (2000b) Morphological relationships of peptidergic and noradrenergic nerve terminals to olivocochlear neurones in the rat. Hear. Res., 144, 53-64.
40. Mulders, W.H. & Robertson, D. (2001) Origin of the noradrenergic innervation of the superior olivary complex in the rat. J. Chem. Neuroanat., 21, 313-322.
41. O'Donnell, P., Lavin, A., Enquist, L.W., Grace, A.A. & Card, J.P. (1997) Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transport of pseudorabies virus. J. Neurosci., 17, 2143-2167.
42. Palkovits, M., Brownstein, M. & Saavedra, J.M. (1974) Serotonin content of the brainstem nuclei in the rat. Brain Res., 80, 237-249.
43. Patuzzi, R.B. & Thompson, M.L. (1991) Cochlear efferent neurons and protection against acoustic trauma: protection of outer hair cell receptor current and interanimal variability, Hear. Res., 54, 45-58.
44. Rajan, R. (1988) Effect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. I. Dependence on electrical stimulation parameters. J. Neurophysiol., 60, 549-568.
45. Robertson, D., Cole, K.S. & Harvey, A.R. (1987) Brainstem organization of efferent projections to the guinea pig cochlea studied using the fluorescent tracers fast blue and diamidino yellow. Exp. Brain. Res., 66, 449-457.
46. Robertson, D. & Mulders, W.H. (2000) Distribution and possible functional roles of some neuractive peptides in the mammalian superior olivary complex. Micr. Res. Techn., 51, 307-317.
47. Robertson, D. & Winter, I.M. (1988) Cochlear nucleus inputs to olivocochlear neurones revealed by combined anterograde and retrograde labelling in the guinea pig. Brain Res., 462, 47-55.
48. Roessner, W. (1965) Stereotaktischer Hirnatlas Vom Meerschweinchen (Stereotaxic Atlas of the Guinea Pig Brain). Pallas Verlag, Lochharn bei München.
49. Roizman, B. & Sears, A.E. (1990) Herpes simplex viruses and their replication. In Fields, B.N. & Knipe, D.M. (Eds), Virology. Raven Press, New York, pp. 1795-1828.
50. Rotto-Percelay, D.M., Wheeler, J.G., Osorio, F.A., Platt, K.B. & Loewy, A.D. (1992) Transneuronal labeling of spinal interneurons and sympathetic preganglionic neurons after pseudorabies virus injections in the rat medial gastrocnemius muscle. Brain. Res., 574, 291-306.
51. Saldana, E., Feliciano, M. & Mugnaini, E. (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J. Comp. Neurol., 371, 15-40.
52. Sams, J.M., Jansen, A.S.P., Mettenleiter, T.C. & Loewy, A.D. (1995) Pseudorabies virus mutants as transneuronal markers. Brain Res., 687, 182.
53. Schaff, B., Magnan, J. & Chays, A. (1997) On the role of the olivocochlear bundle in hearing: 16 case studies. Hear Res., 103, 101-122.
54. Scharf, B., Magnan, J., Collet, L., Ulmer, E. & Chays, A. (1994) On the role of the olivocochlear bundle in hearing: a case study. Hear Res., 75, 11-26.
55. Scharf, B., Nadol, J., Magnan, J., Chays, A. & Marchioni, A. (1993) Does efferent input improve the detection of tones in monaural noise? In Verillo, R. (Ed.), Sensory Research: Multimodal Perspectives. Erlbaum Press, Hillsdale, NJ, pp. 299-306.
56. Shore, S.E., Helfert, R.H., Bledsoe, S.C., Altschuler, R.A. & Godfrey, D.A. (1991) Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig. Hear. Res., 52, 255-268.
57. Spangler, K.M. & Warr, W.B. (1991) The descending auditory system. In Altschuler, R.A. (Ed.), Neurobiology of Hearing: The Central Auditory System. Raven Press, New York, pp. 27-45.
58. Stopp, P.E. (1990) The problem of obtaining reproducible quantitative data of the olivocochlear pathway as exemplified in the guinea pig. Eur. Arch. Otorhinolaryngol., 247, 29-32.
59. Strack, A.M., Sawyer, W.B., Platt, K.B. & Loewy, A.D. (1989) CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain. Res., 491, 274-296.
60. Strick, P.L. & Card, J.P. (1992) Transneuronal mapping of neural circuits with alpha herpes viruses. In Bolam, J.P. (Ed.), Experimental Neuroanatomy: a Practical Approach. Oxford University Press, Oxford, pp. 81-101.
61. Strutz, J. & Bielenberg, K. (1984) Efferent acoustic neurons within the lateral superior olivary nucleus of the guinea pig. Brain Res., 299, 174-177.
62. Strutz, J. & Spatz, W.B. (1980) Superior olivary and extraolivary origin of centrifugal innervation of the cochlea in guinea pig. A horseradish peroxidase study. Neurosci. Lett., 17, 227-230.
63. Sur, J.H. (1995) Study of transneuronal passage of pseudorabies virus in rat central nervous system by use of immunohistochemistry and in situ hybridization. Am. J. Vet. Res., 56, 1195.
64. Syka, J., Popelar, J., Drugs, R. & Vlkova, A. (1990) Descending central auditory pathway-structure and function. In Syka, J. & Masterton, R.B. (Eds), Auditory Pathway - Structure and Function. Plenum Press, New York and London, pp. 279-292.
65. Thompson, A.M., Moore, K.R. & Thompson, G.C. (1995) Distribution and origin of serotoninergic afferents to guinea pig cochlear nucleus. J. Comp. Neurol., 351, 104-116.
66. Thompson, A.M. & Schofield, B.R. (2000) Afferent projections of the superior olivary complex. Microsc. Res. Techn, 51, 330-354.
67. Thompson, A.M. & Thompson, G.C. (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J. Comp. Neurol., 303, 267-285.
68. Thompson, A.M. & Thompson, G.C. (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J. Comp. Neurol., 335, 402-412.
69. Thompson, A.M. & Thompson, G.C. (1995) Light microscopic evidence of serotoninergic projections to olivocochlear neurons in the bush baby (Otolemur garnettii). Brain Res., 695, 263-266.
70. Tomishima, M.J. & Enquist, L.W. (2001) A conserved alpha-herpesvirus protein necessary for axonal localization of viral membrane proteins. J. Cell Biol., 154, 741-752.
71. Ugolini, G. (1995a) Transneuronal tracing with alpha-herpesviruses: a review of methodology. In Kaplitt, M.G. & Loewy, A.D. (Eds), Viral Vectors. Gene Therapy and Neuroscience Applications. Academic Press, New York, pp. 293-317.
72. Ugolini, G. (1995b) Specificity of rabies virus as a transneuronal tracer of motor networks: transfer from hypoglossal motoneurons to connected second-order and higher order central nervous system cell groups. J. Comp. Neurol., 356, 457-480.
73. Versteeg, D.H.G., Gugten, J.V., De Jong, W. & Palkovits, M. (1976) Regional concentrations of noradrenaline and dopamine in rat brain. Brain Res., 113, 563-574.
74. Vetter, D.E., Saldana, E. & Mugnaini, E. (1992) Input from the inferior colliculus to medial olivocochlear neurons in the rat: a double label study with PHA-L and cholera toxin. Hear. Res., 70, 173-186.
75. Walther, J.B. & Rasmussen, G.L. (1960) Descending connections of auditory cortex and thalamus of the cat. Fed. Proc., 19, 291-300.
76. Wang, X. & Robertson, D. (1998) Substance P-sensitive neurones in the rat auditory brainstem: possible relationship to medial olivocochlear neurones. Hear. Res., 116, 86-98.
77. Warr, W.B. (1975) Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J. Comp. Neurol., 161, 159-181.
78. Warr, W.B. (1980) Efferent components of the auditory system. Ann. Otol. Rhinol. Laryngol. Suppl., 89, 114-120.
79. Warr, W.B., Guinan, J.J. & White, J.S. (1986) Organization of the efferent fibers: the lateral and medial olivocochlear systems. In Altschuler, R.A., Hofmann, D.W. & Bobbin, R.P. (Eds), Neurobiology of Hearing: the Cochlea. Raven Press, New York, pp. 333-348.
80. Warren, W.S., Adkison, M.G. & Bartness, T.J. (1996) CNS neurons regulating the sympathetic outflow to white adipose tissue as revealed by transneuronal labeling with pseudorabies virus. Soc. Neurosci. Abstr., 22, 556.9.
81. Weedman, D.L. & Ryugo, D.K. (1996) Projections from auditory cortex to the cochlear nucleus in rats: synapses on granule cell dendrites. J. Comp. Neurol., 371, 311-324.
82. Whealy, M.E., Card, J.P., Robbins, A.K., Dubin, J.R., Rziha, H.J. & Enquist, L.W. (1993) Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins. J. Virol., 67, 3786-3797.
83. Woods, C.I. & Azeredo, W.J. (1999) Noradrenergic and serotoninergic projections to the superior olive: potential for modulation of olivocochlear neurons. Brain Res., 836, 9-18.
84. Wynne, B. & Robertson, D. (1996) Localization of dopamine-β -hydroxylase-like immunoreactivity in the superior olivary complex of the rat. Audiol. Neurootol., 1, 54-64.
85. Xiao, Z. & Suga, N. (2002) Modulation of cochlear hair cells by the auditory cortex in mustached bat. Nature Neurosci., 5, 57-63.
86. Yates, B.J., Smail, J.A., Stocker, S.D. & Card, J.P. (1998) Transneuronal tracing of neural pathways controlling activity of diaphragm motoneurons in the ferret. Neuroscience, 90, 1501-1513.
87. Ye, Y., Machado, D.G. & Kim, D.O. (2000) Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J. Comp. Neurol., 420, 127-138.