Cross-modal interactions of auditory and somatic inputs in the brainstem and midbrain and their imbalance in tinnitus and deafness

American Journal of Audiology

Volumn 17, Issue 2, 2008, Pages

  Dehmel, S ^a   Cui, Y L ^a   Shore, S E ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Auditory system; Cochlear nucleus; Inferior colliculus; Somatosensory system; Tinnitus

Indexed keywords

ANIMAL; ATTENTION; AUDITORY NERVOUS SYSTEM; AUDITORY STIMULATION; BRAIN MAPPING; BRAIN STEM; COCHLEAR NUCLEUS; ELECTROSTIMULATION; HEARING; HEARING IMPAIRMENT; HUMAN; INFERIOR COLLICULUS; MESENCEPHALON; NERVE CELL; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PERCEPTIVE THRESHOLD; PHYSIOLOGY; REVIEW; SENSATION; SENSORY NERVE; SPINAL GANGLION; SYNAPTIC TRANSMISSION; TINNITUS; TRIGEMINUS GANGLION;

ACOUSTIC STIMULATION; AFFERENT PATHWAYS; ANIMALS; ATTENTION; AUDITORY PATHWAYS; AUDITORY PERCEPTION; BRAIN MAPPING; BRAIN STEM; COCHLEAR NUCLEUS; DEAFNESS; ELECTRIC STIMULATION; GANGLIA, SPINAL; HUMANS; INFERIOR COLLICULI; MESENCEPHALON; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; SENSATION; SENSORY THRESHOLDS; SYNAPTIC TRANSMISSION; TINNITUS; TRIGEMINAL GANGLION;

EID: 58749111653     PISSN: 10590889     EISSN: None     Source Type: Journal    
DOI: 10.1044/1059-0889(2008/07-0045)     Document Type: Review

References (106)

1. Adams, J. C. (1983). Multipolar cells in the ventral cochlear nucleus project to the dorsal cochlear nucleus and the inferior colliculus. Neuroscience Letters, 37, 205-208.
2. Aitkin, L. M., Dickhaus, H., Schult, W., & Zimmermann, M. (1978). External nucleus of inferior colliculus: Auditory and spinal somatosensory afferents and their interactions. Journal of Neurophysiology, 41, 837-847.
3. Aitkin, L. M., Kenyon, C. E., & Philpott, P. (1981). The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. The Journal of Comparative Neurology, 196, 25-40.
4. Babic, T., & Ciriello, J. (2004). Medullary and spinal cord projections from cardiovascular responsive sites in the rostral ventromedial medulla. The Journal of Comparative Neurology, 469, 391-412.
5. Bartels, H., Staal, M. J., & Albers, F. W. (2007). Tinnitus and neural plasticity of the brain. Otology & Neurotology, 28(2), 178-184.
6. Batzri-Izraeli, R., Kelly, J. B., Glendenning, K. K., Masterton, R. B., & Wollberg, Z. (1990). Auditory cortex of the long-eared hedgehog (hemiechinus auritus). I. Boundaries and frequency representation. Brain, Behavior and Evolution, 36, 237-248.
7. Bell, C., Bodznick, D., Montgomery, J., & Bastian, J. (1997). The generation and subtraction of sensory expectations within cerebellum-like structures. Brain, Behavior and Evolution, 50(Suppl. 1), 17-31.
8. Bowker, R. M., Westlund, K. N., & Coulter, J. D. (1981). Origins of serotonergic projections to the spinal cord in rat: An immunocytochemical-retrograde transport study. Brain Research, 226(1-2), 187-199.
9. Burian, M., Gstoettner, W., & Zundritsch, R. (1989). Saccular afferent fibers to the cochlear nucleus in the guinea pig. Archives of Oto-rhino-laryngology, 246(5), 238-241.
10. Cacace, A. T. (2003). Expanding the biological basis of tinnitus: Crossmodal origins and the role of neuroplasticity. Hearing Research, 175(1-2), 112-132.
11. Caicedo, A., & Herbert, H. (1993). Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. The Journal of Comparative Neurology, 328, 377-392.
12. Cant, N. B., & Benson, C. G. (2003). Parallel auditory pathways: Projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Research Bulletin, 60, 457-474.
13. Capra, N. F. (1987). Localization and central projections of primary afferent neurons that innervate the temporomandibular joint in cats. Somatosensory Research, 4(3), 201-213.
14. Cui, Y., & Shore, S. E. (2008, February). Topography of projections from the lateral reticular formation and spinal trigeminal nucleus to the cochlear nucleus in guinea pigs. Abstract presented at the meeting of the Association for Research in Otolaryngology, Phoenix, AZ.
15. Darian-Smith, I., Phillips, G., & Ryan, R. D. (1963). Functional organization in the trigeminal main sensory and rostral spinal nuclei of the cat. Journal of Physiology, 168, 129-146.
16. Davis, K. A., Miller, R. L., & Young, E. D. (1996). Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. Journal of Neurophysiology, 76, 3012-3024.
17. Davis, K. A., & Young, E. D. (1997). Granule cell activation of complex-spiking neurons in dorsal cochlear nucleus. Journal of Neuroscience, 17, 6798-6806.
18. Devor, A. (2000). Is the cerebellum like cerebellar-like structures? Brain Research. Brain Research Reviews, 34(3), 149-156.
19. Doucet, J. R., Ross, A. T., Gillespie, M. B., & Ryugo, D. K. (1999). Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus. Journal of Comparative Neurology, 408, 515-531.
20. Eggermont, J. J. (2005). Tinnitus: Neurobiological substrates. Drug Discovery Today, 10, 1283-1290.
21. Ernst, M. O., & Bülthoff, H. H. (2004). Merging the senses into a robust percept. Trends in Cognitive Sciences, 8(4), 162-169.
22. Fremeau, R. T., Jr., Troyer,M. D., Pahner, I., Nygaard, G. O., Tran, C. H., Reimer, R. J., et al. (2001). The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247-260.
23. Gras, C., Herzog, E., Bellenchi,G. C., Bernard, V., Ravassard, P., Pohl, M., et al. (2002). A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. Journal of Neuroscience, 22, 5442-5451.
24. Gstoettner, W., Burian, M., Zundritsch, R., & Mayr, R. (1991). The origin of the vestibulo-cochlear projection in the guinea pig. Neuroscience Letters, 122(2), 163-166.
25. Haenggeli, C. A., Pongstaporn, T., Doucet, J. R., & Ryugo, D. K. (2005). Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat. The Journal of Comparative Neurology, 484, 191-205.
26. Hayashi, H., Sumino, R., & Sessle, B. J. (1984). Functional organization of trigeminal subnucleus interpolaris: Nociceptive and innocuous afferent inputs, projections to thalamus, cerebellum, and spinal cord, and descending modulation from periaqueductal gray. Journal of Neurophysiology, 51, 890-905.
27. Hermann, G. E., Holmes, G. M., Rogers, R. C., Beattie, M. S., & Bresnahan, J. C. (2003). Descending spinal projections from the rostral gigantocellular reticular nuclei complex. The Journal of Comparative Neurology, 455, 210-221.
28. Hsieh, C. Y., & Cramer, K. S. (2006). Deafferentation induces novel axonal projections in the auditory brainstem after hearing onset. The Journal of Comparative Neurology, 497, 589-599.
29. Itoh, K., Kamiya, H., Mitani, A., Yasui, Y., Takada, M., & Mizuno, N. (1987). Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Research, 400, 145-150.
30. Jacquin, M. F., Barcia, M., & Rhoades, R. W. (1989). Structure-function relationships in rat brainstem subnucleus interpolaris: Iv. Projection neurons. The Journal of Comparative Neurology, 282, 45-62.
31. Jain, R., & Shore, S. (2006). External inferior colliculus integrates trigeminal and acoustic information: Unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig. Neuroscience Letters, 395, 71-75.
32. Jousmäki, V., & Hari, R. (1998). Parchment-skin illusion: Sound-biased touch. Current Biology, 8(6), R190.
33. Kaltenbach, J. A. (2006). The dorsal cochlear nucleus as a participant in the auditory, attentional and emotional components of tinnitus. Hearing Research, 216-217, 224-234.
34. Kaltenbach, J. A., Zhang, J., & Afman, C. E. (2000). Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure. Hearing Research, 147(1-2), 282-292.
35. Kaltenbach, J. A., Zhang, J., & Finlayson, P. (2005). Tinnitus as a plastic phenomenon and its possible neural underpinnings in the dorsal cochlear nucleus. Hearing Research, 206(1-2), 200-226.
36. Kamiya, H., Itoh, K., Yasui, Y., Ino, T., & Mizuno, N. (1988). Somatosensory and auditory relay nucleus in the rostral part of the ventrolateral medulla: A morphological study in the cat. The Journal of Comparative Neurology, 273(3), 421-435.
37. Kanold, P. O., & Young, E. D. (2001). Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. Journal of Neuroscience, 21, 7848-7858.
38. Kayser, C., & Logothetis, N. K. (2007). Do early sensory cortices integrate cross-modal information? Brain Structure & Function, 212(2), 121-132.
39. Kevetter, G. A., & Perachio, A. A. (1989). Projections from the sacculus to the cochlear nuclei in the mongolian gerbil. Brain, Behavior and Evolution, 34(4), 193-200.
40. Kim, J. J., Gross, J., Morest, D. K., & Potashner, S. J. (2004). Quantitative study of degeneration and new growth of axons and synaptic endings in the chinchilla cochlear nucleus after acoustic overstimulation. Journal of Neuroscience Research, 77, 829-842.
41. Kim, J. J., Gross, J., Potashner, S. J., & Morest, D. K. (2004). Fine structure of long-term changes in the cochlear nucleus after acoustic overstimulation: Chronic degeneration and new growth of synaptic endings. Journal of Neuroscience Research, 77, 817-828.
42. King, A. J., & Palmer, A. R. (1985). Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Experimental Brain Research, 60, 492-500.
43. Levine, R. A. (1999). Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. American Journal of Otolaryngology, 20, 351-362.
44. Levine, R.A., Abel, M., & Cheng, H. (2003). CNS somatosensory-auditory interactions elicit or modulate tinnitus. Experimental Brain Research, 153, 643-648.
45. Levine, R. A., Nam, E. C., Oron, Y., & Melcher, J. R. (2007). Evidence for a tinnitus subgroup responsive to somatosensory based treatment modalities. Progress in Brain Reserach, 166, 195-207.
46. Lewald, J., Karnath, H. O., & Ehrenstein, W. H. (1999). Neck-proprioceptive influence on auditory lateralization. Experimental Brain Research, 125, 389-396.
47. Li, H., & Mizuno, N. (1997). Single neurons in the spinal trigeminal and dorsal column nuclei project to both the cochlear nucleus and the inferior colliculus by way of axon collaterals: A fluorescent retrograde double-labeling study in the rat. Neuroscience Research, 29(2), 135-142.
48. Lorente de No, R. (1981). The primary acoustic nuclei. New York: Raven Press.
49. Lüthe, L., Häusler, U., & Jürgens, U. (2000). Neuronal activity in the medulla oblongata during vocalization. A single-unit recording study in the squirrel monkey. Behavioural Brain Research, 116(2), 197-210.
50. Meredith, M. A., & Stein, B. E. (1986). Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. Journal of Neurophysiology, 56, 640-662.
51. Michler, S. A., & Illing, R. B. (2002). Acoustic trauma induces reemergence of the growth- and plasticity-associated protein gap-43 in the rat auditory brainstem. The Journal of Comparative Neurology, 451(3), 250-266.
52. Moechars, D., Weston, M. C., Leo, S., Callaerts-Vegh, Z., Goris, I., Daneels, G., et al. (2006). Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. Journal of Neuroscience, 26, 12055-12066.
53. Møller, A. R. (2001). Symptoms and signs caused by neural plasticity. Neurological Research, 23, 565-572.
54. Møller, A. R. (2006). Neural plasticity in tinnitus. Progress in Brain Research, 157, 365-372.
55. Møller, A. R., & Rollins, P. R. (2002). The non-classical auditory pathways are involved in hearing in children but not in adults. Neuroscience Letters, 319, 41-44.
56. Mugnaini, E., & Morgan, J. I. (1987). The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain. Proceedings of the National Academy of Sciences, USA, 84, 8692-8696.
57. Nazruddin, Suemune, S., Shirana, Y., Yamauchi, K., & Shigenaga, Y. (1989). The cells of origin of the hypoglossal afferent nerves and central projections in the cat. Brain Research, 490, 219-235.
58. Nelken, I., & Young, E. D. (1996). Why do cats need a dorsal cochlear nucleus? Journal of Basic and Clinical Physiology and Pharmacology, 7(3), 199-220.
59. Oertel, D., & Young, E. D. (2004). What's a cerebellar circuit doing in the auditory system? Trends in Neuroscience, 27(2), 104-110.
60. Ohlrogge, M., Doucet, J. R., & Ryugo, D. K. (2001). Projections of the pontine nuclei to the cochlear nucleus in rats. The Journal of Comparative Neurology, 436, 290-303.
61. Ostapoff, E. M., Morest, D. K., & Parham, K. (1999). Spatial organization of the reciprocal connections between the cat dorsal and anteroventral cochlear nuclei [see comments]. Hearing Research, 130(1-2), 75-93.
62. Pfaller, K., & Arvidsson, J. (1988). Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. The Journal of Comparative Neurology, 268, 91-108.
63. Pichert, J. W., Hickson, G. B., Bledsoe, S., Trotter, T., & Quinn, D. (1997). Understanding the etiology of serious medical events involving children: Implications for pediatricians and their risk managers. Pediatric Annals, 26(3), 160-164, 167-168, 170-172.
64. Populin, L. C., & Yin, T. C. (2002). Bimodal interactions in the superior colliculus of the behaving cat. Journal of Neuroscience, 22, 2826-2834.
65. Rice, J. J., May, B. J., Spirou, G. A., & Young, E. D. (1992). Pinna-based spectral cues for sound localization in cat. Hearing Research, 58, 132-152.
66. Romfh, J. H., Capra, N. F., & Gatipon, G. B. (1979). Trigeminal nerve and temporomandibular joint of the cat: A horseradish peroxidase study. Experimental Neurology, 65(1), 99-106.
67. Saadé, N. E., Frangieh, A. S., Atweh, S. F., & Jabbur, S. J. (1989). Dorsal column input to cochlear neurons in decerebrate-decerebellate cats. Brain Research, 486, 399-402.
68. Sanchez, T. G., Guerra, G. C., Lorenzi, M. C., Brandão, A. L., & Bento, R. F. (2002). The influence of voluntary muscle contractions upon the onset and modulation of tinnitus. Audiology & Neuro-otology, 7, 370-375.
69. Saunders, J. C. (2007). The role of central nervous system plasticity in tinnitus. Journal of Communication Disorders, 40, 313-334.
70. Shintani, T., Mori, R. L., & Yates, B. J. (2003). Locations of neurons with respiratory-related activity in the ferret brainstem. Brain Research, 974(1-2), 236-242.
71. Shore, S. E. (2005). Multisensory integration in the dorsal cochlear nucleus: Unit responses to acoustic and trigeminal ganglion stimulation. European Journal of Neuroscience, 21, 3334-3348.
72. Shore, S. (in press). Auditory/somatosensory interactions. In G. Adelman & B. H. Smith (Eds.), The new encyclopedia of neuroscience. New York: Elsevier Science.
73. Shore, S. E., DeRidder, D., & Koehler, S. D. (2007). [Stimulation of dorsal root ganglia - effects on DCN neurons]. Unpublished raw data.
74. Shore, S. E., El Kashlan, H., & Lu, J. (2003). Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons. Neuroscience, 119, 1085-1101.
75. Shore, S., Koehler, S., Oldakowski, M., Hughes, L.,& Syed, S. (2008). Dorsal cochlear nucleus reponses to somatosensory stimulation are enhanced after noise-induced hearing loss. European Journal of Neuroscience, 27(1), 155-168.
76. Shore, S. E., Vass, Z., Wys, N. L., & Altschuler, R. A. (2000). Trigeminal ganglion innervates the auditory brainstem. The Journal of Comparative Neurology, 419, 271-285.
77. Shore, S. E., Zeng, C., Zhou, J., & Nannapaneni, N. (2007, November). Deafferentation alters the distribution of vessicular glutamate transporters in the guinea pig cochlear nucleus. Abstract presented at the meeting of the Society for Neuroscience, San Diego, CA.
78. Shore, S. E., & Zhou, J. (2006). Somatosensory influence on the cochlear nucleus and beyond. Hearing Research, 216-217, 90-99.
79. Shore, S., Zhou, J., & Koehler, S. (2007). Neural mechanisms underlying somatic tinnitus. Progress in Brain Research, 166, 107-123.
80. Sola, E., Prestori, F., Rossi, P., Taglietti, V., & D'Angelo, E. (2004). Increased neurotransmitter release during long-term potentiation at mossy fibre-granule cell synapses in rat cerebellum. Journal of Physiology, 557(Pt 3), 843-861.
81. Stanford, T. R., Quessy, S., & Stein, B. E. (2005). Evaluating the operations underlying multisensory integration in the cat superior colliculus. Journal of Neuroscience, 25, 6499-6508.
82. Stein, B. E. (1998). Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Experimental Brain Research, 123(1-2), 124-135.
83. Stein, B. E., & Meredith, M. A. (1993). The merging of the senses. Cambridge, MA: MIT Press.
84. Suemune, S., Nishimori, T., Hosoi, M., Suzuki, Y., Tsuru, H., Kawata, T., et al. (1992). Trigeminal nerve endings of lingual mucosa and musculature of the rat. Brain Research, 586(1), 162-165.
85. Takemura, M., Sugimoto, T., & Shigenaga, Y. (1991). Difference in central projection of primary afferents innervating facial and intraoral structures in the rat. Experimental Neurology, 111, 324-331.
86. Tammer, R., Ehrenreich, L., & Jürgens, U. (2004). Telemetrically recorded neuronal activity in the inferior colliculus and bordering tegmentum during vocal communication in squirrel monkeys (saimiri sciureus). Behavioural Brain Research, 151(1-2), 331-336.
87. Tawil, R. N., Saade, N. E., Bitar, M., & Jabbur, S. J. (1983). Polysensory interactions on single neurons of cat inferior colliculus. Brain Research, 269(1), 149-152.
88. Usunoff, K. G., Marani, E., & Schoen, J. H. (1997). The trigeminal system in man. Advances in Anatomy, Embryology, and Cell Biology, 136, I-X, 1-126.
89. Van Bockstaele, E. J., Pieribone, V. A., & Aston-Jones, G. (1989). Diverse afferents converge on the nucleus paragiganto-cellularis in the rat ventrolateral medulla: Retrograde and anterograde tracing studies. The Journal of Comparative Neurology, 290, 561-584.
90. Varoqui, H., Schäfer, M. K., Zhu, H., Weihe, E., & Erickson, J. D. (2002). Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. Journal of Neuroscience, 22, 142-155.
91. Vass, Z., Shore, S. E., Nuttall, A.L., Jancso, G., Brechtelsbauer, P. B., & Miller, J. M. (1997). Trigeminal ganglion innervation of the cochlea - a retrograde transport study. Neuroscience, 79, 605-615.
92. Vass, Z., Shore, S. E., Nuttall, A. L., & Miller, J. M. (1998). Direct evidence of trigeminal innervation of the cochlear blood vessels. Neuroscience, 84, 559-567.
93. Weedman, D. L., Pongstaporn, T., & Ryugo, D. K. (1996). Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: Mossy fiber endings and their targets. The Journal of Comparative Neurology, 369, 345-360.
94. Weedman, D. L., & Ryugo, D. K. (1996). Projections from auditory cortex to the cochlear nucleus in rats: Synapses on granule cell dendrites. The Journal of Comparative Neurology, 371, 311-324.
95. Weinberg, R. J., & Rustioni, A. (1987). A cuneocochlear pathway in the rat. Neuroscience, 20, 209-219.
96. Winter, I. M., Wiegrebe, L., & Patterson, R. D. (2001). The temporal representation of the delay of iterated rippled noise in the ventral cochlear nucleus of the guinea-pig. Journal of Physiology, 537(Pt 2), 553-566.
97. Wolff, A., & Kunzle, H. (1997). Cortical and medullary somatosensory projections to the cochlear nuclear complex in the hedgehog tenrec. Neuroscience Letters, 221(2-3), 125-128.
98. Wright, D. D., & Ryugo, D. K. (1996). Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. The Journal of Comparative Neurology, 365(1), 159-172.
99. Young, E. D., Nelken, I., & Conley, R. A. (1995). Somatosensory effects on neurons in dorsal cochlear nucleus. Journal of Neurophysiology, 73, 743-765.
100. Young, E. D., Rice, J. J., & Tong, S. C. (1996). Effects of pinna position on head-related transfer functions in the cat. Journal of the Acoustical Society of America, 99, 3064-3076.
101. Zeng, C., Nannapaneni, N., Zhou, J., & Shore, S. (2008, February). Deafferentation changes the distribution of vesicular glutamate transporters associated with auditory nerve or nonauditory inputs to the cochlear nucleus. Abstract presented at the meeting of the Association for Research in Otolaryngology, Phoenix, AZ.
102. Zhan, X., Pongstaporn, T., & Ryugo, D. K. (2006). Projections of the second cervical dorsal root ganglion to the cochlear nucleus in rats. The Journal of Comparative Neurology, 496, 335-348.
103. Zhan, X., & Ryugo, D. K. (2007). Projections of the lateral reticular nucleus to the cochlear nucleus in rats. The Journal of Comparative Neurology, 504, 583-598.
104. Zhou, J., Nannapaneni, N., & Shore, S. (2007). Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus. The Journal of Comparative Neurology, 500, 777-787.
105. Zhou, J., & Shore, S. (2004). Projections from the trigeminal nuclear complex to the cochlear nuclei: A retrograde and anterograde tracing study in the guinea pig. Journal of Neuroscience Research, 78, 901-907.
106. Zhou, J., & Shore, S. (2006). Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig. The Journal of Comparative Neurology, 495, 100-112.