Facilitatory and inhibitory frequency tuning of combination- sensitive neurons in the primary auditory cortex of mustached bats

Journal of Neurophysiology

Volumn 82, Issue 5, 1999, Pages 2327-2345

  Kanwal, Jagmeet S ^a,c   Fitzpatrick, Douglas C ^a,b   Suga, Nobuo ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY ORIENTATION; AUDITORY STIMULATION; BAT; ECHOLOCATION; FACILITATION; FLIGHT; FREQUENCY MODULATION; NONHUMAN; PRIORITY JOURNAL; VELOCITY;

EID: 0032693008     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.82.5.2327     Document Type: Article

References (80)

1. ALLMAN, J. M., MIEZEN, F., AND MCGUINESS, E. Direction and velocity specific surround in three cortical visual areas of the owl monkey. Perception 14: 105-126, 1985.
2. DECHARMS, R. C. AND MERZENICH, M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature 38: 610-613, 1996.
3. EDAMATSU, H., KAWASAKI, M., AND SUGA, N. Distribution of combination-sensitive neurons in the ventral fringe area of the auditory cortex of the mustached bat. J. Neurophysiol. 61: 202-207, 1989.
4. EHRET, G. AND SCHREINER, C. E. Frequency resolution and spectral integration (critical band analysis) in single units of the cat primary auditory cortex. J. Comp. Physiol. [A]. 181: 635-650, 1997.
5. ESSER, K-H. Audio-vocal learning in a non-human mammal: the lesser spearnosed bat Phyllostomus discolor. Neuroreport 5: 1718-1720, 1994.
6. ESSER, K.-H., CONDON, C. J., SUGA, N., AND KANWAL, J. S. Syntax processing by auditory cortical neurons in the FM-FM area of the mustached bat, Pteronotus parnellii. Proc. Natl. Acad. Sci. USA 94: 14019-14024, 1997.
7. EVANS, E. F. AND NELSON, P. G. The responses of single neurones in the cochlear nucleus of the cat as a function of their location and anaesthetic state. Exp. Brain Res. 17: 402-427, 1973.
8. FITZPATRICK, D. C., KANWAL, J., BUTMAN, J. A., AND SUGA, N. Combination-sensitive neurons in the primary auditory cortex of the mustached bat. J. Neurosci. 13: 931-940, 1993.
9. FITZPATRICK, D. C., SUGA, N., AND OLSEN, J. F. Distribution of response types across entire hemispheresof the emustached bat's auditory cortex. J. Comp. Neurol 391: 353-365, 1998.
10. GAIONI, S. J., RIQUIMAROUX, H., AND SUGA, N. Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. J. Neurophysiol. 64: 1801-1817, 1990.
11. GERHARDT, H. C. AND DOHERTY, J. H. Acoustic communication in the gray treefrog, Hyla versicolor, evolutionary and neurobiological implications. J. Comp. Physiol. [A] 162: 261-278, 1988.
12. GRIFFIN, D. Listening in the Dark. New Haven, CT: Yale University Press, 1958.
13. GRIFFIN, D. The importance of atmospheric attenuation for the echolocation of bats (Chiroptera). Anim. Behav. 19: 55-61, 1971.
14. GRIFFIN, D. AND NOVICK, A. Acoustic orientation in neotropical bats. J. Exp. Zool. 130: 251-300, 1955.
15. HARTIGAN, J. A. Clustering Algorithms. New York: John Wiley, 1975.
16. HENSON, O. W., JR., BISHOP, A., KEATING, A., KOBLER, J. B., HENSON, M. M., WILSON, B., AND HANSEN, R. Biosonar imaging of insects by Pteronotus p. parnellii, the mustached bat. Natl. Geogr. Res. 3: 82-101, 1987.
17. HENSON, O. W., JR., HENSON, M. M., KOBLER, J. B., AND POLLAK G. D. The constant frequency component of the biosonar signals of the bat, Pteronotus parnellii parnellii. In: Animal Sonar Systems, edited by R-G. Busnel and J. Fish. New York: Plenum, 1980, p. 913-916.
18. HUFFMAN, R. F. AND HENSON, O. W., JR. Labile cochlear tuning in the mustached bat. I. Concomitant shifts in biosonar emission frequency. J. Comp. Physiol. 171: 725-734.
19. KANWAL, J. S. Processing species-specific calls by combination-sensitive neurons in an echolocating bat. In: The Design of Animal Communication, edited by M. D. Hauser and M. Konishi. Cambridge: MIT Press, 1999, p. 133-157.
20. KANWAL, J. S., FITZPATRICK, D. C., AND SUGA, N. Neurons in the auditory cortex of the mustached bat are sensitive to combinations of non-harmonic frequencies. Soc. Neurosci. Abstr. 17: 444, 1991.
21. KANWAL, J. S., MATSUMURA, S., OHLEMILLER, K. K., AND SUGA, N. Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J. Acoust. Soc. Am. 96: 1229-1254, 1994.
22. KANWAL, J. S., OHLEMILLER, K. K., AND SUGA, N. Selective representation of call-syllables in the DSCF area in the primary auditory cortex of the mustached bat. Soc. Neurosci. Abstr. 18: 884, 1992.
23. KAPADIA, M. K., ITO, M., GILBERT, C. D., AND WESTHEIMER, G. Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron 15: 843-856, 1995.
24. KEATING, A. W., HENSON, O. W., JR., HENSON, M. M., LANCASTER, W. C., AND XIE, D. H. Doppler-Shift compensation by the mustached bat: quantitative data. J. Exp. Biol. 188: 115-129, 1994.
25. KOBLER, J., WILSON, B. S., HENSON, O. W., JR., AND BISHOP, A. L. Echo intensity compensation by echolocating bats. Hear. Res. 20: 99-108, 1985.
26. KICK, S. A. AND SIMMONS, J. A. Automatic gain control in the bat's sonar receiver and the neuroethology of echolocation. J. Neurosci. 4: 2725-2737, 1984.
27. LAWERENCE, B. D. AND SIMMONS, J. A. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J. Acoust. Soc. Am. 71: 585-590, 1982.
28. LOPEZ, P. T. AND NARINS, P. M. Mate choice in the neotropical frog, Eleutherodactylus coqui. Anim. Behav. 41: 757-772, 1991.
29. MAFFEI, L. AND FIORRENTINI, A. The unresponsive regions of visual cortical receptive fields. Vision Res. 16: 1131-1139, 1976.
30. MARGOLIASH, D. AND FORTUNE, E. S. Temporal and harmonic combination-sensitive neurons in the zebra finch's Hvc. J. Neurosci. 12: 4309-4326, 1992.
31. MERZENICH, M. M., KNIGHT, P. L., AND ROTH G. L. Representation of cochlea within the primary auditory cortex in the cat. J. Neurophysiol. 38: 231-249, 1975.
32. MOSS, C. F. AND SCHNITZLER, H.-U. Behavioral studies of auditory information processing. In: Hearing by Bats, edited by A. N. Popper and R. R. Fay. New York: Springer-Verlag, 1995, p. 87-145.
33. NOVICK, A. Pulse duration in the echolocation of insects by the bat, Pteronotus. Ergeb. Biol. 26: 21-26, 1963.
34. NOVICK, A. AND VAISNYS, J. R. Echolocation of flying insects by the bat, Chilonycteris parnelli. Biol. Bull. 127: 478-488, 1964.
35. OHLEMILLER, K. K., KANWAL, J. S., AND SUGA, N. Facilitative responses to species-specific calls in cortical FM-FM neurons of the mustached bat. Neuroreport 7: 1749-1755, 1996.
36. OLSEN, J. F. Processing of biosonar information by the medial geniculate body of the mustached bat, Pteronotus parnellii. PhD thesis, Washington University, 1986.
37. OLSEN, J. F. AND SUGA, N. Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J. Neurophysiol. 65: 1254-1274, 1991.
38. O'NEILL, W. E. AND SUGA, N. Encoding of target range information and its representation in the auditory cortex of the mustached bat. J. Neurosci. 47: 225-255, 1982.
39. PHILLIPS, D. P. AND CYNADER, M. S. Some neural mechanisms in the cat's auditory cortex underlying sensitivity to combined tone and wide-sepctrum noise stimuli. Hear. Res. 18: 87-102, 1985.
40. 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.
41. PHILLIPS, D. P., SEMPLE, M. N., CALFORD, M. B., AND KITZES, L. M. Level dependent representation of stimulus frequency in the cat's primary auditory cortex. Exp. Brain Res. 102: 210-226, 1994.
42. RAUSCHECKER, J. P. Cortical processing of complex sounds. Curr. Opin. Neurobiol. 8: 516-21, 1998.
43. RAUSCHECKER, J. P., TIAN, B., AND HAUSER, M. Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268: 111-114, 1995.
44. REALE, R. A. AND IMIG, T. J. Tonotopic organization in auditory cortex of the cat. J. Comp. Neurol. 192: 265-291, 1980.
45. RIQUIMAROUX, H., GAIONI, S. J., AND SUGA, N. Cortical computational maps control auditory perception. Science 251: 565-568, 1991.
46. ROMANI, G. C., WILLIAMSON, S. J., AND KAUFMAN, L. Tonotopic organization of the human auditory cortex. Science 216: 1339-1340, 1982.
47. SCHREINER, C. E. Functional topographies in the primary auditory cortex of the cat. Acta Otolaryngol. Suppl. 16.491: P7-15, 1992.
48. SCHREINER, C. E. Order and disorder in auditory cortical maps. Curr. Opin. Neurobiol. 5: 489-496, 1995
49. SCHREINER, C. E. AND CYNADER, M. S. Basic functional organization of secondary auditory cortical field (AII) of the cat. J. Neurophysiol. 51: 1284-1305, 1984.
50. SCHREINER, C. E. AND MENDELSON, J. R. Functional topography of cat primary auditory cortex: distribution of integrated excitation. J. Neurophysiol. 64: 1442-1459, 1990.
51. 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.
52. SCHREINER, C. E. AND SUTTER, M. L. Topography of excitatory bandwidth in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. J. Neurophysiol. 68: 1487-1503, 1992.
53. SHAMMA, S., FLESHMAN, J., WISER, P., AND VERSNEL, H. Organization of response areas in ferret primary auditory cortex. J. Neurophysiol. 69: 367-383, 1993.
54. SHOFNER, W. P. AND YOUNG, E. D. Excitatory/inhibitory response types in the cochlear nucelus. Relationships to discharge patterns and responses to electrical stimulation of the auditory nerve. J. Neurophysiol. 54: 917-939, 1985.
55. SUGA, N. Functional properties of auditory neurons in the cortex of echolocating bats. J. Physiol. (Lond.) 181: 681-700, 1965.
56. SUGA, N. Amplitude-spectrum representation in the Doppler-shifted CF processing area of the auditory cortex of the mustache bat. Science 196: 64-67, 1977.
57. SUGA, N. Functional organization of the auditory cortex representation beyond tonotopy in the bat. In: Cortical Sensory Organization: Multiple Auditory Areas, edited by C. N. Woolsey and N. J. Clifton. New Jersey: Humana, 1982, vol. 3, p. 157-218.
58. SUGA, N. The extent to which biosonar information is represented in the bat auditory cortex. In: Dynamic Aspects of Neocortical Function, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: John Wiley, 1984, p. 315-373.
59. SUGA, N. AND HORIKAWA, H. Multiple time axes for representation of echo delays in the auditory cortex of the mustached bat. J. Neurophysiol. 55: 776-805, 1986.
60. SUGA, N. AND JEN, P.H.-S. Disproportionate tonotopic representation for processing species-specific CF-FM sonar signals in mustache bat auditory cortex. Science 194: 542-544, 1976.
61. SUGA, N. AND KANWAL, J. S. Echolocation: creating computational maps. In: Handbook of Brain Theory and Neural Networks, edited by M. A. Arbib. Cambridge, MA: MIT Press, 1995, p. 344-348.
62. SUGA, N. AND MANABE, T. Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J. Neurophysiol. 47: 225-255, 1982.
63. SUGA, N., NIWA, H., TANIGUCHI, I., AND MARGOLIASH, D. The personalized auditory cortex of the mustached bat: adaptation for echolocation. J. Neurophysiol. 58: 643-654, 1987.
64. SUGA, N. AND O'NEILL, W. E. Neural axis representing target range in the auditory cortex of the mustached bat. Science 206: 351-353, 1979.
65. SUGA, N. AND O'NEILL, W. E. Auditory processing of echoes: representation of acoustic information from the environment in the bat cerebral cortex. In: Animal Sonar Systems, edited by R. G. Busnel and J. F. Fish. New York: Plenum, 1980, p. 589-611.
66. SUGA, N., O'NEILL, W. E., KUJIRAI, K., AND MANABE, T. Specialization of "combination-sensitive" neurons for processing of complex biosonar signals in the auditory cortex of the rnustached bat. J. Neurophysiol. 49: 1573-1626, 1983.
67. SUGA, N. AND SCHLEGEL, P. Neural attenuation of responses to emitted sounds in echolocating bats. Science 177: 82-84, 1972.
68. SUGA, N. AND TSUZUKI, K. Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustache bat. J. Neurophysiol. 53: 1109-1144, 1985.
69. SUGA, N., ZHANG, Y., AND YAN, J. Cortical maps for hearing and egocentric selection for self-organization. Trends Cognit. Sci. 1: 13-20, 1997.
70. SUTTER, M. L. AND SCHREINER, C. E. Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J. Neurophysiol. 65: 1207-1226, 1991.
71. SUTTER, M. L. AND SCHREINER, C. E. Topography of intensity tuning in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. J. Neurophysiol. 73: 190-204, 1995.
72. TAKAHASHI, T. Time-variant structure of auditory cortex of the macaque monkey. Neurosci. Lett. 187: 1-4, 1995.
73. TANIGUCHI, I., ARAI, O., AND SAITO, N. Functional laminar and columnar organization of the auditory centers in echolocating Japanese greater horseshoe bats. Neurosci. Lett. 88: 17-20, 1988.
74. TRAPPE, M. AND SCHNITZLER, H.-U. Doppler-shift compensation in insect catching horseshoe bats. Naturwissenschaften 69S: 193-194, 1982.
75. TUNTURI, A. R. A difference in the representation of auditory signals for the left and right ears in the iso-frequency contours of the right middle ectosylvian auditory cortex of the dog. Am. J. Physiol. 168: 712-727, 1952.
76. WANG, X., MERZENICH, M. M., BEITEL, R., AND SCHREINER, C. E. Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J. Neurophysiol. 74: 685-706, 1995.
77. WILKINSON, L., ENGELMAN, L., CORTER, J., AND COWARD, M. Cluster Analysis. In: Systat 8.0: Statistics, edited by L. Wilkinson. Chicago: SPSS Inc., 1998, p. 53-86.
78. YOUNG, E. D. AND BROWNELL, W. E. Responses to tones and noise of single cells in dorsal coclear nucleus of unanesthetized cata. J. Neurophysiol. 39: 282-299, 1976.
79. ZHANG, Y. AND SUGA, N. Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J. Neurophysiol. 78: 3489-3492, 1997.
80. ZHANG, Y., SUGA, N., AND YAN, J. Corticofugal modulation of frequency processing in bat auditory system. Nature 387: 900-903, 1997.