Cortical synthesis of azimuth-sensitive single-unit responses with nonmonotonic level tuning: A thalamocortical comparison in the cat

Journal of Neurophysiology

Volumn 75, Issue 3, 1996, Pages 1206-1220

  Barone, Pascal ^a,b   Clarey, Janine C ^a,c   Irons, W Andrew ^a,d   Imig, Thomas J ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b INSERM   (France)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF WISCONSIN LA CROSSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC NERVE FIBER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; CAT; DIRECTIONAL HEARING; MEDIAL GENICULATE BODY; NERVE PROJECTION; NOISE; NONHUMAN; PRIORITY JOURNAL; SOUND DETECTION; SOUND PRESSURE; THALAMOCORTICAL TRACT;

EID: 0029871342     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.75.3.1206     Document Type: Article

References (88)

1. AITKIN, L. M. Rate-level functions of neurons in the inferior colliculus of cats measured with the use of free-field sound stimuli. J. Neurophysiol. 65: 383-392, 1991.
2. AITKIN, L. M. AND DUNLOP, C. W. Interplay of excitation and inhibition in the cat medial geniculate body. J. Neurophysiol. 31: 44-61, 1968.
3. AITKIN, L. M., GATES, G. R., AND PHILLIPS, S. C. Responses of neurons in inferior colliculus to variations in sound-source azimuth. J. Neurophysiol. 52: 1-17, 1984.
4. AITKIN, L. M. AND MARTIN, R. L. The representation of stimulus azimuth by high best-frequency azimuth-selective neurons in the central nucleus of the inferior colliculus of the cat. J. Neurophysiol. 57: 1185-1200, 1987.
5. AITKIN, L. M. AND PRAIN, S. M. Medial geniculate body: unit responses in the awake cat. J. Neurophysiol. 37: 512-521, 1974.
6. ANDERSEN, R. A., ROTH, G. L., AITKIN, L. M., AND MERZENICH, M. M. 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.
7. BARONE, P., IRONS, W. A., CLAREY, J. C., AND IMIG, T. J. A comparison of the directional properties of nonmonotonic neurons in the auditory thalamus and primary auditory cortex (A1) of cat. Soc. Neurosci. Abstr. 16: 719, 1990.
8. BENSON, D. A., HIENZ, R. D., AND GOLDSTEIN, M. H., JR. Single-unit activity in the auditory cortex of monkeys actively localizing sound sources: spatial tuning and behavioral dependency. Brain Res. 219: 249-267, 1981.
9. BENSON, D. A. AND TEAS, D. C. Single unit study of binaural interaction in the auditory cortex of the chinchilla. Brain Res. 103: 313-338, 1976.
10. BERMAN, A. L. AND JONES, E. G. The Thalamus and Basal Telencephalon of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates. Madison, WI: Univ. of Wisconsin Press, 1982.
11. BOCH, G. R., WEBSTER, W. R., AND AITKIN, L. M. Discharge patterns of single units in inferior colliculus of the alert cat. J. Neurophysiol. 35: 265-277, 1972.
12. BOUDREAU, J. C. AND TSUCHITANI, C. Binaural interaction in the cat superior olive S segment. J. Neurophysiol. 31: 442-454, 1968.
13. BRUGGE, J. F., DUBROVSKY, N. A., AITKIN, L M., AND ANDERSON, D. J. Sensitivity of single neurons in auditory cortex of cat to binaural tonal stimulation; effects of varying interaural time and intensity. J. Neurophysiol. 32: 1005-1024, 1969.
14. BRUGGE, J. F. AND MERZENICH, M. M. Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J. Neurophysiol. 36: 1138-1158, 1973.
15. CALFORD, M. B. The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J. Neurosci. 3. 2350-2364, 1983.
16. CALFORD, M. B., MOORE, D. R., AND HUTCHINGS, M. E. Central and peripheral contributions to coding of acoustic space by neurons in inferior colliculus of cat. J. Neurophysiol. 55: 587-603, 1986.
17. CLAREY, J. C., BARONE, P., AND IMIG, T. J. Functional organization of sound direction and sound pressure level in primary auditory cortex of the cat. J. Neurophysiol. 72: 2383-2405, 1994.
18. EISENMAN, L. M. Neural encoding of sound location: an electrophysiological study in auditory cortex (AI) of the cat using free field stimuli. Brain Res. 75: 203-214, 1974.
19. EVANS, E. F. Cortical representation. In: Hearing Mechanisms in Vertebrates, edited by A. V. S. De Reuck and J. Knight. Boston, MA: Little, Brown, 1968, p. 272-287.
20. FAINGOLD, C. L., BOERSMA ANDERSON, C. A., AND CASPARY, D. M. Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear. Res. 52: 201-216, 1991.
21. FAINGOLD, C. L., BOERSMA ANDERSON, C. A., AND RANDALL, M. E. Stimulation or blockade of the dorsal nucleus of the lateral lemniscus alters binaural and tonic inhibition in contralateral inferior colliculus neurons. Hear. Res. 69: 98-106, 1993.
22. FUZESSERY, Z. M., WENSTRUP, J. J., AND POLLAK, G. D. Determinants of horizontal sound location selectivity in binaurally excited neurons in an isofrequency region of the mustache bat inferior colliculus. J. Neurophysiol. 63: 1128-1147, 1990.
23. GODFREY, D. A., KLANG, N. Y. S., AND NORRIS, B. E. Single unit activity in the posteroventral cochlear nucleus of the cat. J. Comp. Neurol. 162: 247-268, 1975a.
24. GODFREY, D. A., KIANG, N. Y. S., AND NORRIS, B. E. Single unit activity in the dorsal cochlear nucleus of the cat. J. Comp. Neurol. 162: 269-284, 1975b.
25. GOLDBERG, J. M. AND BROWN, P. B. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 32: 613-636, 1969.
26. GOLDBERG, J. M. AND BROWNELL, W. E. Discharge characteristics of neurons in anteroventral and dorsal cochlear nuclei of cat. Brain Res. 64: 35-54, 1973.
27. HEIL, P., RAJAN, R., AND IRVINE, D. R. F. Topographic representation of tone intensity along the isofrequency axis of cat primary auditory cortex. Hear. Res. 76: 188-202, 1994.
28. HIRSCH, J. A., CHAN, J. C. K., AND YIN, T. C. T. Responses of neurons in the cat's superior colliculus to acoustic stimuli. I. Monaural and binaural response properties. J. Neurophysiol. 53: 726-745, 1985.
29. IMIG, T. J., IRONS, W. A., AND SAMSON, F. A. Single-unit selectivity to azimuthal direction and sound pressure level of noise bursts in cat high-frequency primary auditory cortex. J. Neurophysiol. 63: 1448-1466, 1990
30. IMIG, T. J. AND MOREL, A. Tonotopic organization in ventral nucleus of medial geniculate body in the cat. J. Neurophysiol. 53: 309-340, 1985a.
31. IMIG, T. J. AND MOREL, A. Tonotopic organization in lateral part of posterior group of thalamic nuclei in the cat. J. Neurophysiol. 53: 836-851, 1985b.
32. IRONS, W. A., II Directional Selectivity of Single Units in the Auditory Thalamus of Cats (PhD dissertation). Lawrence, KS: Univ. of Kansas, 1989.
33. IRVINE, D. R. F. Progress in Sensory Physiology 7: The Auditory Brainstem. New York: Springer-Verlag, 1986, p. 227.
34. IRVINE, D. R. F. Interaural intensity differences in the cat: changes in sound pressure level at the two ears associated with azimuthal displacements in the frontal horizontal plane. Hear. Res. 26: 267-286, 1987.
35. IRVINE, D. R. F. AND 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.
36. IVARSSON, C., DE RIBAUPIERRE, Y., AND DE RIBAUPIERRE, F. Influence of auditory localization cues on neuronal activity in the auditory thalamus of the cat. J. Neurophysiol. 59: 586-606, 1988.
37. KAUTZ, D. W. AND WAGNER, H. Neuronal mechanisms of auditory motion direction sensitivity. Soc. Neurosci. Abstr. 20: 320, 1994.
38. KITZES, L. M. AND DOHERTY, D. Influence of callosal activity on units in the auditory cortex of ferret (Mustela putorius). J. Neurophysiol. 71: 1740-1751, 1994.
39. KITZES, L. M., WRENGE, K. S., AND CASSADY, J. M. Patterns of responses of cortical cells to binaural stimulation. J. Comp. Neurol. 192: 455-472, 1980.
40. KUDO, M. AND NIIMI, K. Ascending projections of the inferior colliculus onto the medial geniculate body in the cat studied by anterograde and retrograde tracing techniques. Brain Res. 155: 113-117, 1978.
41. KUDO, M. AND NIIMI, K. Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J. Comp. Neurol. 191: 545-556, 1980.
42. LI, L. AND KELLY, J. B. Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus. J. Neurosci. 12: 4530-4539, 1992.
43. MERRILL, E. G. AND AINSWORTH, A. Glass-coated platinum-plated tungsten microelectrodes. Med. Biol. Eng. 10: 662-697, 1972.
44. MIDDLEBROOKS, J. C. Binaural mechanisms of spatial tuning in the cat's superior colliculus distinguished using monaural occlusion. J. Neurophysiol. 57: 688-701, 1987.
45. MIDDLEBROOKS, J. C. AND PETTIGREW, J. D. Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location. J. Neurosci. 1: 107-120, 1981.
46. MOREL, A. AND IMIG, T. J. Thalamic projections to fields A. AI. P, and VP in the cat auditory cortex. J. Comp. Neurol. 265: 119-144, 1987.
47. NELKEN, I. AND YOUNG, E. D. Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli. J. Neurophysiol. 71: 2446-2462, 1994.
48. PALMER, A. R. AND EVANS, E. F. Cochlear fibre rate-intensity functions: no evidence for basilar membrane nonlinearities. Hear. Res. 2: 319-326, 1980.
49. PARK, T. J. AND POLLAK, G. D. GABA shapes sensitivity to interaural intensity disparities in the mustache bat's inferior colliculus: implications for encoding sound location. J. Neurosci. 13: 2050-2067, 1993a.
50. PARK, T. J. AND POLLAK, G. D. GABA shapes topographic organization of response latency in the mustache bat's inferior colliculus. J. Neurosci. 13: 5172-5187, 1993b.
51. PARK, T. J. AND POLLAK, G. D. Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat. J. Neurophysiol. 72: 1080-1102, 1994.
52. PFINGST, B. E. AND O'CONNOR, T A. Characteristics of neurons in auditory cortex of monkeys performing a simple auditory task. J. Neurophysiol. 45: 16-34, 1981.
53. PHILLIPS, D. P. Stimulus intensity and loudness recruitment: neural correlates. J. Acoust. Soc. Am. 82: 1-12, 1987.
54. PHILLIPS, D. P. AND IRVINE, D R F. Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. J. Neurophysiol. 45: 48-58, 1981a.
55. PHILLIPS, D. P. AND IRVINE, D. R. F. Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural intensity differences. Hear. Res. 4: 229-307, 1981b.
56. PHILLIPS, D. P. AND ORMAN, S. S. Responses of single neurons in posterior field of cat auditory cortex to tonal stimulation. J. Neurophysiol. 51: 147-163, 1984.
57. PHILLIPS, D. P., ORMAN, S. S., MUSICANT, A. D., AND WILSON, G. F. Neurons in the cat's primary auditory cortex distinguished by their responses to tones and wide-spectrum noise. Hear. Res. 18. 73-86, 1985.
58. PRIETO, J. E., PETERSON, B. A., AND WINER, J. A. Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). J. Comp. Neurol. 344: 349-382, 1994.
59. RAJAN, R., AITKIN, L. M., AND IRVINE, D. R. F. Azimuthal sensitivity of neurons in primary auditory cortex of cats. II. Organization along frequency-band strips. J. Neurophysiol. 64: 888-902, 1990a.
60. RAJAN, R., AITKIN, L. M., IRVINE, D. R. F., AND MCKAY, J. Azimuthal sensitivity of neurons in primary auditory cortex of cats. I. Types of sensitivity and the effects of variations in stimulus parameters J. Neurophysiol. 64: 872-887, 1990b.
61. RITZ, L A. AND BROWELL, W. E. Single unit analysis of the posteroventral cochlear nucleus of the decerebrate cat. Neuroscience 7: 1995-2010, 1982.
62. RODRIGUES-DAGAEFF, C., SIMM, G., DE RIEAUPIERRE, Y., VILLA, A., DE RIBAUPIERRE, F., AND ROUILLER, E M. Functional organization of the ventral division of the medial geniculate body of the cat: evidence for a rostrocaudal gradient of response properties and cortical projections. Hear. Res. 39: 103-126, 1989.
63. ROSE, J. E., GREENWOOD, D. D., GOLDBERG, J. M., AND HIND, J. E. 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.
64. ROUILLER, E. M., CAPT, M., HORNUNG, J. P., AND STREIT, P. Correlation between regional changes in the distributions of GABA-containing neurons and unit response properties in the medial geniculate body of the cat. Hear. Res 49: 249-258, 1990.
65. ROUILLER, E. M., DE RIBAUPIERRE, Y., MOREL, A., AND DE RIBAUPIERRE, F. Intensity functions of single unit responses to tone in the medial geniculate body of cat. Hear. Res. 11: 235-247, 1983
66. RYAN, A. AND MILLER, J. Single unit responses in the inferior colliculus of the awake and performing rhesus monkey. Exp. Brain Res. 32: 389-407, 1978.
67. SACHS, M. B. AND ABBAS, P. J. Rate versus level function for auditory-nerve fibers in cats: tone-burst stimuli. J. Acoust Soc. Am. 56: 1835-1847, 1974.
68. SAMSON, F. K , BARONE, P., CLAREY, J. C., AND IMIG, T. J. Effects of ear plugging on single-unit azimuth sensitivity in cat primary auditory cortex II. Azimuth sensitivity dependent upon binaural stimulation. J. Neurophysiol. 71: 2194-2216, 1994.
69. SAMSON, F. K., CLAREY, J. C., BARONE, P., AND IMIG T. J. Effects of ear plugging on single-unit azimuth sensitivity in cat primary auditory cortex. I. Evidence for monaural directional cues. J. Neurophysiol. 70: 492-511, 1993.
70. SCHREINER, C. E., MENDELSON, J. R., AND SUTTER, M. L. Functional topography of cat primary auditory cortex: representation of tone intensity. Exp. Brain Res. 92: 105-122, 1992.
71. SEMPLE, M. N., AITKIN, L. M., CALFORD, M. B., PETTIGREW, J. D., AND PHILLIPS, D. P. Spatial receptive fields in the cat inferior colliculus. Hear. Res. 10: 203-225, 1983.
72. SEMPLE, M. N. AND KITZES, L. M. Single-unit responses in the inferior colliculus: differential consequences of contralateral and ipsilateral auditory stimulation. J. Neurophysiol. 53: 1467-1482, 1985.
73. SEMPLE, M. N. AND KITZES, L. M. Binaural processing of sound pressure level in the inferior colliculus. J. Neurophysiol. 57: 1130-1147, 1987.
74. SEMPLE, M. N. AND KITZES, L. M. Processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute rather than interaural level differences. J Neurophysiol. 69: 449-461, 1993a.
75. SEMPLE, M. N. AND KITZES, L. M. Processing of sound pressure level in cat primary auditory cortex: two-way intensity network tuning. J. Neurophysiol. 69: 462-473, 1993b.
76. SMITH, R. L. Encoding of sound intensity by auditory neurons. In: Auditory Function: Neurobiological Bases of Hearing, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1988, p. 243-274.
77. SPITZER, M. W. AND SEMPLE, M. N. Responses of inferior colliculus neurons to time-varying interaural phase disparity, effects of shifting the locus of virtual motion. J. Neurophysiol. 69: 1245-1263, 1993.
78. STANFORD, T. R., KUWADA, S., AND BATRA, R. A comparison of the interaural time sensitivity of neurons in the inferior colliculus and thalamus of the unanesthetized rabbit. J. Neurosci. 12: 3200-3216, 1992.
79. SUGA, N. Amplitude-spectrum representation in the Doppler-shifted-CF processing area of the auditory cortex of the mustache bat. Science Wash DC 196: 64-67, 1977.
80. SUGA, N. AND MANABE, T. Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J. Neurophysiol. 47: 225-255, 1982.
81. TAKAHASHI, T., MOISEFF, A., AND KONISHI, M. Time and intensity cues are processed independently in the auditory system of the owl. J. Neurosci 4 1781-1786, 1984
82. WHITFIELD, I. C. AND PURSER, D. Microelectrode study of the medial geniculate body in unanesthetized free-moving cats. Brain Behav. Evol. 6: 311-322, 1972.
83. WISE, L. Z. AND IRVINE, D. R F Interaural intensity difference sensitivity based on facilitatory binaural interaction in cat superior colliculus. Hear Res. 16: 181-187, 1984.
84. WISE, L. Z. AND IRVINE, D. R. F. Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus. implications for auditory spatial representation. J. Neurophysiol. 54: 185-211, 1985.
85. YANG, L., POLLAK, G. D., AND RESLER, C. GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat's inferior colliculus. J. Neurophysiol. 68: 1760-1774, 1992.
86. YIN, T. C. T. AND CHAN, J. C. K. Neural mechanisms underlying interaural time sensitivity to tones and noise. In: Auditory Function - Neurobiological Bases of Hearing, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1988, p 385-430.
87. YOUNG, E. D. AND BROWELL, W. E. Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J. Neurophysiol. 39 282-300, 1976.
88. YOUNG, E. D., SHOFNER, W. P., WHITE, J. A., ROBERT, J.-M., AND VOIGT, H. F. Response properties of cochlear nucleus neurons in relationship to physiological mechanisms. In: Auditory Function: Neurobiological Bases of Hearing, edited by G. M Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1988, chapt. 9, p. 277-312.