Auditory cortical responses to electrical stimulation of the inferior colliculus: Implications for an auditory midbrain implant

Journal of Neurophysiology

Volumn 96, Issue 3, 2006, Pages 975-988

  Lim, Hubert H ^a   Anderson, David J ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; SILICON;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY THRESHOLD; COCHLEA; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED RESPONSE AUDIOMETRY; FREQUENCY ANALYSIS; GUINEA PIG; HEARING; HEARING AID; HISTOGRAM; IMPLANT; INFERIOR COLLICULUS; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; SUPERIOR COLLICULUS; TONOTOPY;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; COCHLEAR IMPLANTS; ELECTRIC STIMULATION; GUINEA PIGS; INFERIOR COLLICULUS; MODELS, ANIMAL;

EID: 33748317747     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01112.2005     Document Type: Article

References (112)

1. Aitkin LM and Phillips SC. Is the inferior colliculus an obligatory relay in the cat auditory system? Neurosci Lett 44: 259-264, 1984.
2. Andersen RA, Roth GL, Aitkin LM, and Merzenich MM. The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J Comp Neurol 194: 649-662, 1980.
3. Anderson DJ, Najafi K, Tanghe SJ, Evans DA, Levy KL, Hetke JF, Xue XL, Zappia JJ, and Wise KD. Batch-fabricated thin-film electrodes for stimulation of the central auditory system. IEEE Trans Biomed Eng 36: 693-704, 1989.
4. Anderson MJ and Young ED. Isoflurane/N2O anesthesia suppresses narrow-band but not wideband inhibition in dorsal cochlear nucleus. Hear Res 188: 29-41, 2004.
5. Arenberg JG, Furukawa S, and Middlebrooks JC. Auditory cortical images of tones and noise bands. J Assoc Res Otolaryngol 1: 183-194, 2000.
6. Bagshaw EV and Evans MH. Measurement of current spread from microelectrodes when stimulating within the nervous system. Exp Brain Res 25: 391-400, 1976.
7. Bajo VM and Moore DR. Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. J Comp Neurol 486: 101-116, 2005.
8. Beebe X and Rose TL. Charge injection limits of activated iridium oxide electrodes with 0.2 ms pulses in bicarbonate buffered saline. IEEE Trans Biomed Eng 35: 494-495, 1988.
9. Beitel RE, Snyder RL, Schreiner CE, Raggio MW, and Leake PA. Electrical cochlear stimulation in the deaf cat: comparisons between psychophysical and central auditory neuronal thresholds. J Neurophysiol 83: 2145-2162, 2000.
10. Benabid AL, Chabardes S, and Seigneuret E. Deep-brain stimulation in Parkinson's disease: long-term efficacy and safety - what happened this year? Curr Opin Neurol 18: 623-630, 2005.
11. Bierer JA and Middlebrooks JC. Auditory cortical images of cochlear-implant stimuli: dependence on electrode configuration. J Neurophysiol 87: 478-492, 2002.
12. Boockvar JA, Telfeian A, Baltuch GH, Skolnick B, Simuni T, Stern M, Schmidt ML, and Trojanowski JQ. Long-term deep brain stimulation in a patient with essential tremor: clinical response and postmortem correlation with stimulator termination sites in ventral thalamus. Case report. J Neurosurg 93: 140-144, 2000.
13. Brackmann DE, Hitselberger WE, Nelson RA, Moore J, Waring MD, Portillo F, Shannon RV, and Telischi FF. Auditory brainstem implant: I. Issues in surgical implantation. Otolaryngol Head Neck Surg 108: 624-633, 1993.
14. Britten KH, Shadlen MN, Newsome WT, and Movshon JA. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12: 4745-4765, 1992.
15. Brunso-Bechtold JK, Thompson GC, and Masterton RB. HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197: 705-722, 1981.
16. Calford MB and Aitkin LM. Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3: 2365-2380, 1983.
17. Cant NB and Benson CG. Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60: 457-474, 2003.
18. Cant NB and Benson CG. Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): differences in distribution of projections from the cochlear nuclei and the superior olivary complex. J Comp Neurol 495: 511-528, 2006.
19. Casseday JH, Fremouw T, and Covey E. The inferior colliculus: a hub for the central auditory system. In: Springer Handbook of Auditory Research: Integrative Functions in the Mammalian Auditory Pathway, edited by Oertel D, Fay RR, and Popper AN. New York: Springer-Verlag, 2002, vol. 15, p. 238-318.
20. Chase SM and Young ED. Limited segregation of different types of sound localization information among classes of units in the inferior colliculus. J Neurosci 25: 7575-7585, 2005.
21. Colletti V and Shannon RV. Open set speech perception with auditory brainstem implant? Laryngoscope 115: 1974-1978, 2005.
22. Dobelle WH, Stensaas SS, Mladejovsky MG, and Smith JB. A prosthesis for the deaf based on cortical stimulation. Ann Otol Rhinol Laryngol 82: 445-463, 1973.
23. Drake KL, Wise KD, Farraye J, Anderson DJ, and BeMent SL. Performance of planar multisite microprobes in recording extracellular single-unit intracortical activity. IEEE Trans Biomed Eng 35: 719-732, 1988.
24. Drennan WR and Pfingst BE. Current-level discrimination using bipolar and monopolar electrode configurations in cochlear implants. Hear Res 202: 170-179, 2005.
25. Ehret G. The auditory midbrain, a "shunting yard" of acoustical information processing. In: The Central Auditory System, edited by Ehret G and Romand R. New York: Oxford Univ. Press, 1997, p. 259-316.
26. Evans DG, Huson SM, Donnai D, Neary W, Blair V, Teare D, Newton V, Strachan T, Ramsden R, and Harris R. A genetic study of type 2 neurofibromatosis in the United Kingdom. I. Prevalence, mutation rate, fitness, and confirmation of maternal transmission effect on severity. J Med Genet 29: 841-846, 1992.
27. Evans EF and Nelson PG. The responses of single neurones in the cochlear nucleus of the cat as a function of their location and the anaesthetic state. Exp Brain Res 17: 402-427, 1973.
28. Faye-Lund H. The neocortical projection to the inferior colliculus in the albino rat. Anat Embryol (Berl) 173: 53-70, 1985.
29. Feliciano M and Potashner SJ. Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus. J Neurochem 65: 1348-1357, 1995.
30. Friesen LM, Shannon RV, Baskent D, and Wang X. Speech recognition in noise as a function of the number of spectral channels: comparison of acoustic hearing and cochlear implants. J Acoust Soc Am 110: 1150-1163, 2001.
31. Gaese BH and Ostwald J. Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. J Neurophysiol 86: 1062-1066, 2001.
32. Gaese BH and Ostwald J. Complexity and temporal dynamics of frequency coding in the awake rat auditory cortex. Eur J Neurosci 18: 2638-2652, 2003.
33. Geniec P and Morest DK. The neuronal architecture of the human posterior colliculus. A study with the Golgi method. Acta Otolaryngol Suppl 295: 1-33, 1971.
34. Green D and Swets J. Signal Detection Theory and Psychophysics. New York: Wiley, 1966.
35. Helfert RH and Aschoff A. Superior olivary complex and nuclei of the lateral lemniscus. In: The Central Auditory System, edited by Ehret G and Romand R. New York: Oxford Univ. Press, 1997, p. 193-258.
36. Herbert H, Aschoff A, and Ostwald J. Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304: 103-122, 1991.
37. Howard MA, Volkov IO, Mirsky R, Garell PC, Noh MD, Granner M, Damasio H, Steinschneider M, Reale RA, Hind JE, and Brugge JF. Auditory cortex on the human posterior superior temporal gyrus. J Comp Neurol 416: 79-92, 2000.
38. Huffman RF and Henson OW Jr. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Brain Res Rev 15: 295-323, 1990.
39. Jolly CN, Spelman FA, and Clopton BM. Quadrupolar stimulation for cochlear prostheses: modeling and experimental data. IEEE Trans Biomed Eng 43: 857-865, 1996.
40. Kaku Y, Yonekawa Y, and Taub E. Transcollicular approach to intrinsic tectal lesions. Neurosurgery 44: 338-343; discussion 343-334, 1999.
41. Kelly JB and Caspary DM. Pharmacology of the inferior colliculus. In: The Inferior Colliculus, edited by Winer JA and Schreiner CE. New York: Springer Science/Business Media, 2005, p. 248-281.
42. Kral A, Hartmann R, Mortazavi D, and Klinke R. Spatial resolution of cochlear implants: the electrical field and excitation of auditory afferents. Hear Res 121: 11-28, 1998.
43. Langner G. Periodicity coding in the auditory system. Hear Res 60: 115-142, 1992.
44. Langner G and Schreiner CE. Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60: 1799-1822, 1988.
45. Lenarz M, Reuter G, Patrick J, and Lenarz T. Auditory midbrain implant - design and evaluation. Assoc Res Otolaryngol Abstr 27: 160, 2004.
46. Lenarz T, Reuter G, Paasche G, Lenarz M, Gibson P, and Mackiewicz M. Auditory midbrain implant (AMI) - Ein neues therapiekonzept fur neurale taubheit. HNO Info 28: 146, 2003.
47. Lim HH and Anderson DJ. Feasibility experiments for the development of a midbrain auditory prosthesis. Proc 1st Int IEEE EMBS Conf Neural Eng, Capri Island, Italy, 2003, p. 193-196.
48. Loftus WC, Bishop DC, Saint Marie RL, and Oliver DL. Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. J Comp Neurol 472: 330-344, 2004.
49. Loizou PC, Dorman M, and Fitzke J. The effect of reduced dynamic range on speech understanding: implications for patients with cochlear implants. Ear Hear 21: 25-31, 2000.
50. Lu T, Liang L, and Wang X. Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat Neurosci 4: 1131-1138, 2001.
51. Lu T and Wang X. Information content of auditory cortical responses to time-varying acoustic stimuli. J Neurophysiol 91: 301-313, 2004.
52. Malmierca MS, Rees A, Le Beau FE, and Bjaalie JG. Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357: 124-144, 1995.
53. McIntyre CC and Grill WM. Selective microstimulation of central nervous system neurons. Ann Biomed Eng 28: 219-233, 2000.
54. McIntyre CC and Grill WM. Finite element analysis of the current-density and electric field generated by metal microelectrodes. Ann Biomed Eng 29: 227-235, 2001.
55. Merzenich MM and Reid MD. Representation of the cochlea within the inferior colliculus of the cat. Brain Res 77: 397-415, 1974.
56. Middlebrooks JC, Dykes RW, and Merzenich MM. Binaural response-specific bands in primary auditory cortex (AI) of the cat: topographical organization orthogonal to isofrequency contours. Brain Res 181: 31-48, 1980.
57. Middlebrooks JC and Zook JM. Intrinsic organization of the cat's medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex. J Neurosci 3: 203-224, 1983.
58. Mitani A and Shimokouchi M. Neuronal connections in the primary auditory cortex: an electrophysiological study in the cat. J Comp Neurol 235: 417-429, 1985.
59. Mitani A, Shimokouchi M, and Nomura S. Effects of stimulation of the primary auditory cortex upon colliculogeniculate neurons in the inferior colliculus of the cat. Neurosci Lett 42: 185-189, 1983.
60. Najafi K, Wise KD, and Mochizuki T. A high-yield IC-compatible multichannel recording array. IEEE Trans Electron Dev 32: 1206-1211, 1985.
61. Nelson DA, Schmitz JL, Donaldson GS, Viemeister NF, and Javel E. Intensity discrimination as a function of stimulus level with electric stimulation. J Acoust Soc Am 100: 2393-2414, 1996.
62. Oliver DL. Neuronal organization in the inferior colliculus. In: The Inferior Colliculus, edited by Winer JA and Schreiner CE. New York: Springer Science/Business Media, 2005, p. 69-114.
63. Oliver DL, Beckius GE, Bishop DC, and Kuwada S. Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of cat. J Comp Neurol 382: 215-229, 1997.
64. Otto KJ, Rousche PJ, and Kipke DR. Cortical microstimulation in auditory cortex of rat elicits best-frequency dependent behaviors. J Neural Eng 2: 42-51, 2005a.
65. Otto KJ, Rousche PJ, and Kipke DR. Microstimulation in auditory cortex provides a substrate for detailed behaviors. Hear Res 210: 112-117, 2005b.
66. Otto SR, Brackmann DE, Hitselberger WE, Shannon RV, and Kuchta J. Multichannel auditory brainstem implant: update on performance in 61 patients. J Neurosurg 96: 1063-1071, 2002.
67. Penfield W and Perot P. The brain's record of auditory and visual experience. A final summary and discussion. Brain 86: 595-696, 1963.
68. Pfingst BE, Burnett PA, and Sutton D. Intensity discrimination with cochlear implants. J Acoust Soc Am 73: 1283-1292, 1983.
69. Raggio MW and Schreiner CE. Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. I. Intensity dependence of firing rate and response latency. J Neurophysiol 72: 2334-2359, 1994.
70. Raggio MW and Schreiner CE. Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. III. Activation patterns in short- and long-term deafness. J Neurophysiol 82: 3506-3526, 1999.
71. Ramachandran R and May BJ. Functional segregation of ITD sensitivity in the inferior colliculus of decerebrate cats. J Neurophysiol 88: 2251-2261, 2002.
72. Ranck JB Jr. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98: 417-440, 1975.
73. Rauschecker JP and Shannon RV. Sending sound to the brain. Science 295: 1025-1029, 2002.
74. Redies H, Brandner S, and Creutzfeldt OD. Anatomy of the auditory thalamocortical system of the guinea pig. J Comp Neurol 282: 489-511, 1989a.
75. Redies H, Sieben U, and Creutzfeldt OD. Functional subdivisions in the auditory cortex of the guinea pig. J Comp Neurol 282: 473-488, 1989b.
76. Ritz LA and Brownell WE. Single unit analysis of the posteroventral cochlear nucleus of the decerebrate cat. Neuroscience 7: 1995-2010, 1982.
77. Rodrigues-Dagaeff C, Simm G, De Ribaupierre Y, Villa A, De Ribaupierre F, and Rouiller EM. Functional organization of the ventral division of the medial geniculate body of the cat: evidence for a rostro-caudal gradient of response properties and cortical projections. Hear Res 39: 103-125, 1989.
78. Romand R and Avan P. Anatomical and functional aspects of the cochlear nucleus. In: The Central Auditory System, edited by Ehret G and Romand R. New York: Oxford Univ. Press, 1997, p. 97-191.
79. Ronner SF, Foote WE, and Pollen DA. Intracortical microstimulation of neurons in the visual cortex of the cat. Electroencephalogr Clin Neurophysiol 52: 375-377, 1981.
80. Rose HJ and Metherate R. Thalamic stimulation largely elicits orthodromic, rather than antidromic, cortical activation in an auditory thalamocortical slice. Neuroscience 106: 331-340, 2001.
81. Rose JE, Greenwood DD, Goldberg JM, and Hind JE. Some discharge characteristics of single neurons in the inferior colliculus of the cat. I. Tonotopical organization, relation of spike-counts to tone intensity, and firing patterns of single elements. J Neurophysiol 26: 294-320, 1963.
82. Roth GL, Aitkin LM, Andersen RA, and Merzenich MM. Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182: 661-680, 1978.
83. Rousche PJ, Otto KJ, Reilly MP, and Kipke DR. Single electrode microstimulation of rat auditory cortex: an evaluation of behavioral performance. Hear Res 179: 62-71, 2003.
84. Rutkowski RG, Wallace MN, Shackleton TM, and Palmer AR. Organisation of binaural interactions in the primary and dorsocaudal fields of the guinea pig auditory cortex. Hear Res 145: 177-189, 2000.
85. Schofield BR, Hallman LE, and Lin CS. Morphology of corticotectal cells in the primary visual cortex of hooded rats. J Comp Neurol 261: 85-97, 1987.
86. Schreiner CE and Langner G. Laminar fine structure of frequency organization in auditory midbrain. Nature 388: 383-386, 1997.
87. Schwartz MS, Otto SR, Brackmann DE, Hitselberger WE, and Shannon RV. Use of a multichannel auditory brainstem implant for neurofibromatosis type 2. Stereotact Funct Neurosurg 81: 110-114, 2003.
88. Semple MN and Aitkin LM. Representation of sound frequency and laterality by units in central nucleus of cat inferior colliculus. J Neurophysiol 42: 1626-1639, 1979.
89. Serviere J, Webster WR, and Calford MB. Isofrequency labelling revealed by a combined [14C]-2-deoxyglucose, electrophysiological, and horseradish peroxidase study of the inferior colliculus of the cat. J Comp Neurol 228: 463-477, 1984.
90. Shannon RV, Fayad J, Moore J, Lo WW, Otto S, Nelson RA, and O'Leary M. Auditory brainstem implant: II. Postsurgical issues and performance. Otolaryngol Head Neck Surg 108: 634-642, 1993.
91. Shannon RV, Fu QJ, and Galvin J 3rd. The number of spectral channels required for speech recognition depends on the difficulty of the listening situation. Acta Otolaryngol Suppl: 50-54, 2004.
92. Shneiderman A and Henkel CK. Banding of lateral superior olivary nucleus afferents in the inferior colliculus: a possible substrate for sensory integration. J Comp Neurol 266: 519-534, 1987.
93. Simmons FB, Mongeon CJ, Lewis WR, and Huntington DA. Electrical stimulation of acoustical nerve and inferior colliculus. Arch Otolaryngol 79: 559-568, 1964.
94. Skinner MW, Arndt PL, and Staller SJ. Nucleus 24 advanced encoder conversion study: performance versus preference. Ear Hear 23: 2S-17S, 2002.
95. Snyder RL, Bierer JA, and Middlebrooks JC. Topographic spread of inferior colliculus activation in response to acoustic and intracochlear electric stimulation. J Assoc Res Otolaryngol 5: 305-322, 2004.
96. Spelman FA. The past, present, and future of cochlear prostheses. IEEE Eng Med Biol Mag 18: 27-33, 1999.
97. Stiebler I and Ehret G. Inferior colliculus of the house mouse. I. A quantitative study of tonotopic organization, frequency representation, and tonethreshold distribution. J Comp Neurol 238: 65-76, 1985.
98. Suga N, Gao E, Zhang Y, Ma X, and Olsen JF. The corticofugal system for hearing: recent progress. Proc Natl Acad Sci USA 97: 11807-11814, 2000.
99. Syka J, Popelar J, Kvasnak E, and Astl J. Response properties of neurons in the central nucleus and external and dorsal cortices of the inferior colliculus in guinea pig. Exp Brain Res 133: 254-266, 2000.
100. Syka J, Suta D, and Popelar J. Responses to species-specific vocalizations in the auditory cortex of awake and anesthetized guinea pigs. Hear Res 206: 177-184, 2005.
101. Torterolo P, Zurita P, Pedemonte M, and Velluti RA. Auditory cortical efferent actions upon inferior colliculus unitary activity in the guinea pig. Neurosci Lett 249: 172-176, 1998.
102. Velenovsky DS, Cetas JS, Price RO, Sinex DG, and McMullen NT. Functional subregions in primary auditory cortex defined by thalamocortical terminal arbors: an electrophysiological and anterograde labeling study. J Neurosci 23: 308-316, 2003.
103. Vollmer M, Beitel RE, and Snyder RL. Auditory detection and discrimination in deaf cats: psychophysical and neural thresholds for intracochlear electrical signals. J Neurophysiol 86: 2330-2343, 2001.
104. Wallace MN, Rutkowski RG, and Palmer AR. Identification and localisation of auditory areas in guinea pig cortex. Exp Brain Res 132: 445-456, 2000.
105. Weiland JD and Anderson DJ. Chronic neural stimulation with thin-film, iridium oxide electrodes. IEEE Trans Biomed Eng 47: 911-918, 2000.
106. Winer JA. The human medial geniculate body. Hear Res 15: 225-247, 1984.
107. Winer JA. Three systems of descending projections to the inferior colliculus. In: The Inferior Colliculus, edited by Winer JA and Schreiner CE. New York: Springer Science/Business Media, 2005, p. 231-247.
108. Winer JA, Chernock ML, Larue DT, and Cheung SW. Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey. Hear Res 168: 181-195, 2002.
109. Winer JA, Larue DT, Diehl JJ, and Hefti BJ. Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400: 147-174, 1998.
110. Yan J and Ehret G. Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci 16: 119-128, 2002.
111. Zeng FG and Galvin JJ 3rd. Amplitude mapping and phoneme recognition in cochlear implant listeners. Ear Hear 20: 60-74, 1999.
112. Zurita P, Villa AE, de Ribaupierre Y, de Ribaupierre F, and Rouiller EM. Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions. Neurosci Res 19: 303-316, 1994.