Sensitivity of cochlear nucleus neurons to spatio-temporal changes in auditory nerve activity

Journal of Neurophysiology

Volumn 108, Issue 12, 2012, Pages 3172-3195

  Wang, Grace I ^a,b,c   Delgutte, Bertrand ^a,c,d  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b Department of Electrical Engineering and Computer Science   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anesthetized cat; Auditory nerve; Cochlear nucleus; Coincidence detection; Spatio temporal pattern

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; COCHLEAR NERVE; COCHLEAR NUCLEUS; CONTROLLED STUDY; EXPERIMENTAL CAT; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SPIKE; TONOTOPY;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; CATS; COCHLEAR NERVE; COCHLEAR NUCLEUS; NEURONS; TIME FACTORS;

EID: 84871258679     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00160.2012     Document Type: Article

References (89)

1. Babalian AL, Jacomme AV, Doucet JR, Ryugo DK, Rouiller EM. Commissural glycinergic inhibition of bushy and stellate cells in the anteroventral cochlear nucleus. Neuroreport 13: 555-558, 2002.
2. Blackburn CC, Sachs MB. Classification of unit types in the anteroventral cochlear nucleus: post-stimulus time histograms and regularity analysis. J Neurophysiol 62: 1303-1329, 1989.
3. Bourk TR. Electrical Responses of Neural Units in the Anteroventral Cochlear Nucleus of the Cat (PhD thesis). Cambridge, MA: MIT, 1976.
4. Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B. Precise inhibition is essential for microsecond interaural time difference coding. Nature 417: 543-547, 2002.
5. Bruce IC, Sachs MB, Young ED. An auditory-periphery model of the effects of acoustic trauma on auditory nerve responses. J Acoust Soc Am 113: 369-388, 2003.
6. Cai Y, Walsh EJ, McGee J. Mechanisms of onset responses in octopus cells of the cochlear nucleus: implications of a model. J Neurophysiol 78: 872-883, 1997.
7. Cant NB. The fine structure of two types of stellate cells in the anterior division of the anteroventral cochlear nucleus of the cat. Neuroscience 104: 2308-2320, 1981.
8. Cant NB, Morest DK. Organization of the neurons in the anterior division of the anteroventral cochlear nucleus of the cat. Light-microscopic observations. J Neurosci 4: 1909-1923, 1979.
9. Carlyon RP, Datta AJ. Masking period patterns of Schroeder-phase complexes: effects of level, number of components, and phase of flanking components. J Acoust Soc Am 101: 3648-3657, 1997.
10. Carlyon RP, Long CJ, Micheyl C. Across-channel timing differences as a potential code for the frequency of pure tones. J Assoc Res Otolaryngol 13: 159-171, 2012.
11. Carlyon RP, Shamma S. An account of monaural phase sensitivity. J Acoust Soc Am 114: 333-348, 2003.
12. Carney LH. Sensitivities of cells in anteroventral cochlear nucleus of cat to spatiotemporal discharge patterns across primary afferents. J Neurophysiol 64: 437-456, 1990.
13. Carney LH. Modelling the sensitivity of cells in the anteroventral cochlear nucleus to spatiotemporal discharge patterns. Philos Trans R Soc Lond B Biol Sci 336: 405-406, 1992.
14. Carney LH. A model for the responses of low-frequency auditory-nerve fibers in cat. J Acoust Soc Am 93: 401-417, 1993.
15. Carney LH. Spatio-temporal encoding of sound level: models for normal encoding and recruitment of loudness. Hear Res 76: 31-44, 1994.
16. Carney LH, Yin TC. Temporal coding of resonances by low-frequency auditory nerve fibers: single-fiber responses and a population model. J Neurophysiol 60: 1653-1677, 1988.
17. Cedolin L, Delgutte B. Spatio-temporal representation of the pitch of harmonic complex tones in the auditory nerve. J Neurosci 30: 12712-12724, 2010.
18. Day M, Semple M. Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays. J Neurophysiol 106: 1985-1999, 2011.
19. Evans EF, Zhao W. Varieties of inhibition in the processing and control of processing in the mammalian cochlear nucleus. Prog Brain Res 97: 117-126, 1993.
20. Finlayson PG, Caspary DM. Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. J Neurophysiol 65: 598-605, 1991.
21. Gai Y, Carney LH. Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. J Neurophysiol 99: 1077-1095, 2008.
22. Glendenning KK, Hutson KA, Nudo RJ, Masterton RB. Acoustic chiasm. II. Anatomical basis of binaurality in lateral superior olive of cat. J Comp Neurol 232: 261-285, 1985.
23. Glendenning KK, Masterton RB, Baker BN, Wenthold RJ. Acoustic chiasm. III. Nature, distribution, and sources of afferents to the lateral superior olive in the cat. J Comp Neurol 310: 377-400, 1991.
24. Hewitt MJ, Meddis R, Shacketon TM. A compute model of a cochlearnucleus stellate cell: responses to amplitude-modulated and pure-tone stimuli. J Acoust Soc Am 91: 2096-2109, 1992.
25. Huffman DA. The generation of impulse-equivalent pulse trains. IRE Trans IT 8: S10-S16, 1962.
26. Irvine DR, Gago G. Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences. J Neurophysiol 63: 570-591, 1990.
27. Johnson DH, Swami A. The transmission of signals by auditory-nerve fiber discharge patterns. J Acoust Soc Am 74: 493-501, 1983.
28. Joris PX, Carney LH, Smith PH, Yin TC. Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71: 1022-1036, 1994a.
29. Joris PX, Carney LH, Smith PH, Yin TC. Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J Neurophysiol 71: 1037-1051, 1994b.
30. Joris PX, Smith PH. The volley theory and the spherical cell puzzle. Neuroscience 154: 65-76, 2008.
31. Joris PX, Yin TC. Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J Neurophysiol 73: 1043-1062, 1995.
32. Kalluri S, Delgutte B. Mathematical models of cochlear nucleus onset neurons. I. Point neuron with many weak synaptic inputs. J Comp Neurol 14: 71-90, 2003a.
33. Kalluri S, Delgutte B. Mathematical models of cochlear nucleus onset neurons. II. Model with dynamic spike-blocking state. J Comp Neurol 14: 91-110, 2003b.
34. Kiang NY, Moxon EC, Levine RA. Auditory-nerve activity in cats with normal and abnormal cochleas. In: Sensorineural Hearing Loss, edited by Wolstenholme GE, Knight J. London: Churchill, 1970, p. 241-267.
35. Kohlrausch A, Sander A. Phase effects in masking related to dispersion in the inner ear. II. Masking period patterns of short targets. J Acoust Soc Am 97: 1817-1829, 1995.
36. Kopp-Scheinpflug C, Dehmel S, Dorrscheidt GJ, Rubsamen R. Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. J Neurosci 22: 11004-11018, 2002.
37. Krips R, Furst M. Stochastic properties of coincidence-detector neural cells. Neural Comput 21: 2524-2553, 2009.
38. Larsen E, Cedolin L, Delgutte B. Pitch representations in the auditory nerve: two concurrent complex tones. J Neurophysiol 100: 1301-1319, 2008.
39. Laudanski J, Coombes S, Palmer AR, Sumner CJ. Mode-locked spike trains in responses of ventral cochlear nucleus chopper and onset neurons to periodic stimuli. J Neurophysiol 103: 1226-1237, 2010.
40. Levy KL, Kipke DR. Mechanisms of the cochlear nucleus octopus cell's onset response: synaptic effectiveness and threshold. J Acoust Soc Am 103: 1940-1950, 1998.
41. Liberman MC. Central projections of auditory-nerve fibers of differing spontaneous rate. II. Posteroventral and dorsal cochlear nuclei. J Comp Neurol 327: 17-36, 1993.
42. McGinley MJ, Liberman MC, Bal R, Oertel D. Generating synchrony from the asynchronous: compensation for cochlear traveling wave delays by the dendrites of individual brainstem neurons. J Neurosci 32: 9301-9311, 2012.
43. Molnar CE, Pfeiffer RR. Interpretation of spontaneous spike discharge patterns of neurons in the cochlear nucleus. Proc IEEE 56: 993-1004, 1968.
44. Needham K, Paolini AG. Fast inhibition underlies the transmission of auditory information between cochlear nuclei. J Neurosci 23: 6357-6361, 2003.
45. Oertel D, Bal R, Gardner SM, Smith PH, Joris PX. Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proc Natl Acad Sci USA 97: 11773-11779, 2000.
46. Oertel D, Wickesberg RE. Glycinergic inhibition in the cochlear nuclei: evidence for tuberculoventral neurons being glycinergic. In: The Mammalizan Cochlear Nuclei: Organization and Function, edited by Merchan MA, Juiz JJ, Godfrey DA, Mugnaini E. New York: Plenum, 1993, p. 225-238.
47. Ostapoff EM, Benson CG, Saint Marie RL. GABA-and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J Comp Neurol 381: 500-512, 1997.
48. Palmer AR, Shackleton TM. Variation in the phase of response to lowfrequency pure tones in the guinea pig auditory nerve as functions of stimulus level and frequency. J Assoc Res Otolaryngol 10: 233-250, 2009.
49. Paolini AG, FitzGerald JV, Burkitt AN, Clark GM. Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat. Hear Res 159: 101-116, 2001.
50. Papoulis A. The Fourier Integral and Its Applications. New York McGraw Hill, 1962.
51. Park TJ, Klug A, Holinstat M, Grothe B. Interaural level difference processing in the lateral superior olive and the inferior colliculus. J Neurophysiol 92: 289-301, 2004.
52. Patterson JH, Green DM. Discrimination of transient signals having identical energy spectra. J Acoust Soc Am 48: 894-905, 1970.
53. Patterson JH, Ronken DA, Green DM. Phase perception of transient signals having identical power spectra. J Acoust Soc Am 46: 121, 1969.
54. Pecka M, Brand A, Behrend O, Grothe B. Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition. J Neurosci 28: 6914-6925, 2008.
55. Redd EE, Cahill HB, Pongstaporn T, Ryugo DK. The effects of congenital deafness on auditory nerve synapses: type I and type II multipolar cells in the anteroventral cochlear nucleus of cats. J Assoc Res Otolaryngol 3: 403-417, 2002.
56. Rhode WS, Smith PH. Encoding timing and intensity in the ventral cochlear nucleus of the cat. J Neurophysiol 56: 261-286, 1986.
57. Roberts M, Golding N. Reassessing the role of inhibition in the MSO (Abstract). Assoc Res Otolaryngol 122, 2012.
58. Rothman JS, Young ED, Manis PB. Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. J Neurophysiol 70: 2562-2583, 1993.
59. Ryugo DK, Sento S. Synaptic connections of the auditory nerve in cats: relationship between endbulbs of Held and spherical bushy cells. J Comp Neurol 305: 35-48, 1991.
60. Sakoe H, Chiba S. Dynamic programming algorithm optimization for spoken word recognition. IEEE Trans Acoust Speech 26: 43-49, 1978.
61. Sayles M, Winter IM. The temporal representation of the delay of dynamic iterated rippled noise with positive and negative gain by single units in the ventral cochlear nucleus. Brain Res 1171: 52-66, 2007.
62. Semple MN, Kitzes LM. Binaural processing of sound pressure level in the inferior colliculus. J Neurophysiol 57: 1130-1147, 1987.
63. Sento S, Ryugo DK. Endbulbs of Held and spherical bushy cells in cats: morphological correlates with physiological properties. J Comp Neurol 280: 553-562, 1989.
64. Shamma S. Speech processing in the auditory system. II. Lateral inhibition and the central processing of speech evoked activity in the auditory nerve. J Acoust Soc Am 78: 1622-1632, 1985.
65. Shamma S, Shen N, Gopalaswamy P. Stereausis: binaural processing without neural delays. J Acoust Soc Am 86: 989-1006, 1989.
66. Shera CA, Guinan JJ Jr. Stimulus-frequency-emission delay: a test of coherent reflection filtering and a window on cochlear tuning. J Acoust Soc Am 113: 2762-2772, 2003.
67. Shofner WP. Responses of cochlear nucleus units in the chinchilla to iterated rippled noises: analysis of neural autocorrelograms. J Neurophysiol 81: 2662-2674, 1999.
68. Smith PH, Joris PX, Carney LH, Yin TC. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304: 387-407, 1991.
69. Smith PH, Joris PX, Yin TC. Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331: 245-260, 1993.
70. Smith PH, Joris PX, Yin TC. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body of the cat. J Neurophysiol 79: 3127-3142, 1998.
71. Smith PH, Rhode WS. Characterization of HRP-labelled globular bushy cells in the cat anteroventral cochlear nucleus. J Comp Neurol 266: 360-375, 1987.
72. Spirou GA, Rager J, Manis PB. Convergence of auditory-nerve fiber projections onto globular bushy cells. Neuroscience 136: 843-863, 2005.
73. Tolbert LP, Morest DK. The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: electron microscopy. Neuroscience 7: 3053-3068, 1982a.
74. Tolbert LP, Morest DK. The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Golgi and Nissl methods. Neuroscience 7: 3013-3030, 1982b.
75. Tollin DJ, Yin TC. Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25: 10648-10657, 2005.
76. Tsai JJ, Koka K, Tollin DJ. Varying overall sound intensity to the two ears impacts interaural level difference discrimination thresholds by single neurons in the lateral superior olive. J Neurophysiol 103: 875-886, 2010.
77. van der Heijden M, Joris PX. Panoramic measurements of the apex of the cochlea. J Neurosci 26: 11462-11473, 2006.
78. van Gisbergen JA, Grashuis JL, Johannesma PI, Vendrick AJ. Statistical analysis and interpretation of the initial response of cochlear nucleus neurons to tone bursts. Exp Brain Res 23: 407-423, 1975.
79. Wenstrup JJ, Fuzessery ZM, Pollak GD. Binaural neurons in the mustache bat's inferior colliculus. I. Responses of 60 kHz EI units to dichotic sound stimulation. J Neurophysiol 60: 1369-1383, 1988.
80. Wenthold RJ. Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunocytochemical and retrograde transport study. Brain Res 415: 183-187, 1987.
81. Wickesberg RE, Oertel D. Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J Neurosci 10: 1762-1768, 1990.
82. Yin TC, Chan JC. Interaural time sensitivity in medial superior olive of cat. J Neurophysiol 64: 465-488, 1990.
83. Young ED, Robert JM, Shofner WP. Regularity and latency of units in the ventral cochlear nucleus: implications for unit classification and generation of response properties. J Neurophysiol 60: 1-29, 1988.
84. Young ED, Sachs MB. Auditory nerve inputs to cochlear nucleus neurons studied with cross-correlation. Neuroscience 154: 127-138, 2008.
85. Zhang X, Heinz MG, Bruce IC, Carney LH. A phenomenological model for the responses of auditory-nerve fibers. I. Nonlinear tuning with compression and suppression. J Acoust Soc Am 109: 648-670, 2001.
86. Zilany MS, Bruce IC. Modeling auditory-nerve responses for high sound pressure levels in the normal and impaired auditory periphery. J Acoust Soc Am 120: 1446-1466, 2006.
87. Zilany MS, Bruce IC. Representation of the vowel // in normal and impaired auditory nerve fibers: model predictions of responses in cats. J Acoust Soc Am 122: 402-417, 2007.
88. Zilany MS, Bruce IC, Nelson PC, Carney LH. A phenomenological model of the synapse between the inner hair cell and auditory nerve: long-term adaptation with power-law dynamics. J Acoust Soc Am 126: 2390-2412, 2009.
89. Zweig G. Basilar membrane motion. Cold Spring Harb Symp Quant Biol 40: 619-633, 1976.