Patterned tone sequences reveal non-linear interactions in auditory spectrotemporal receptive fields in the inferior colliculus

Hearing Research

Volumn 267, Issue 1-2, 2010, Pages 96-110

  Brimijoin, W Owen ^a   O'Neill, William E ^a,b  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY SPECTROTEMPORAL RECEPTIVE FIELD; AUDITORY STIMULATION; BAT; CONTROLLED STUDY; CORRELATION ANALYSIS; EVOKED AUDITORY RESPONSE; FREQUENCY MODULATOR; INFERIOR COLLICULUS; MALE; NONHUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; SOUND DETECTION; SPEECH; SPIKE WAVE; VOCALIZATION; ANIMAL; ANIMAL MODEL; AUDITORY NERVOUS SYSTEM; HEARING; NERVE CELL; NONLINEAR SYSTEM; PATTERN RECOGNITION; PHYSIOLOGY;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; AUDITORY PERCEPTION; CHIROPTERA; INFERIOR COLLICULI; MALE; MODELS, ANIMAL; NEURONS; NONLINEAR DYNAMICS; PATTERN RECOGNITION, PHYSIOLOGICAL;

EID: 77953547748     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2010.04.005     Document Type: Article

References (79)

1. Aertsen A., Johannesma P., Hermes D. Spectro-temporal receptive fields of auditory neurons in the grassfrog. II. Biol. Cybern. 1980, 38:235-248.
2. Ahrens M.B., Linden J.F., Sahani M. Nonlinearities and contextual influences in auditory cortical responses modeled with multilinear spectrotemporal methods. J. Neurosci. 2008, 28:1929-1942.
3. Andoni S., Li N., Pollak G.D. Spectrotemporal receptive fields in the inferior colliculus revealing selectivity for spectral motion in conspecific vocalizations. J. Neurosci. 2007, 27:4882-4893.
4. Atencio C.A., Blake D.T., Strata F., Cheung S.W., Merzenich M.M., Schreiner C.E. Frequency-modulation encoding in the primary auditory cortex of the awake owl monkey. J. Neurophysiol. 2007, 98:2182-2195.
5. Bar-Yosef O., Rotman Y., Nelken I. Responses of neurons in cat primary auditory cortex to bird chirps: effects of temporal and spectral context. J. Neurosci. 2002, 22:8619-8632.
6. Barbour D.L., Wang X. Auditory cortical responses elicited in awake primates by random spectrum stimuli. J. Neurosci. 2003, 23:7194-7206.
7. Brand A., Urban R., Grothe B. Duration tuning in the mouse auditory midbrain. J. Neurophysiol. 2000, 84:1790-1799.
8. Brimijoin W.O., O'Neill W.E. On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus. Hear. Res. 2005, 210:63-79.
9. Britt R., Starr A. Synaptic events and discharge patterns of cochlear nucleus cells. II. Frequency modulated tones. J. Neurophysiol. 1976, 39:179-194.
10. Brosch M., Schreiner C.E. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 1997, 77:923-943.
11. Brosch M., Schreiner C.E. Sequence sensitivity of neurons in cat primary auditory cortex. Cerebral Cortex 2000, 10:1155-1167.
12. Calford M.B., Semple M.N. Monaural inhibition in cat auditory cortex. J. Neurophysiol. 1995, 73:1876-1891.
13. Casseday J.H., Ehrlich D., Covey E. Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 1994, 264:847-850.
14. Christianson G.B., Sahani M., Linden J.F. The consequences of response nonlinearities for interpretation of spectrotemporal receptive fields. J. Neurosci. 2008, 28:446-455.
15. Covey E., Kauer J.A., Casseday J.H. Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J. Neurosci. 1996, 16:3009-3018.
16. de Bruijn N.G. A Combinatorial Problem. Koninklijke Nederlandse Akademie v Wetenschappen 1946, 49(49):758-764.
17. de Charms R.C., Blake D.T., Merzenich M.M. Optimizing sound features for cortical neurons. Science 1998, 280:1439-1443.
18. Depireux D.A., Simon J.Z., Klein D.J., Shamma S.A. Spectro-temporal response feld characterization with dynamic ripples in ferret primary auditory cortex. J. Neurophysiol. 2001, 85:1220-1234.
19. Eggermont J.J., Aertsen A.M., Hermes D.J., Johannesma P.I. Spectro-temporal characterization of auditory neurons: redundant or necessary. Hear. Res. 1981, 5:109-121.
20. Escabi M.A., Schreiner C.E. Nonlinear spectrotemporal sound analysis by neurons in the auditory midbrain. J. Neurosci. 2002, 22:4114-4131.
21. Faure P.A., Fremouw T., Casseday J.H., Covey E. Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J. Neurosci. 2003, 23:3052-3065.
22. Fitzpatrick D.C., Kanwal J.S., Butman J.A., Suga N. Combination-sensitive neurons in the primary auditory cortex of the mustached bat. J. Neurosci. 1993, 13:931-940.
23. Fritz J.B., Shamma S.A., Elhilali M., Klein D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat. Neurosci. 2003, 6:1216-1223.
24. Fritz J.B., Elhilali M., Shamma S.A. Differential dynamic plasticity of A1 receptive fields during multiple spectral tasks. J. Neurosci. 2005, 25:7623-7635.
25. Fuzessery Z.M. Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus. J. Neurophysiol. 1994, 72:1061-1079.
26. Fuzessery Z.M., Hall J.C. Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J. Neurophysiol. 1996, 76:1059-1073.
27. Fuzessery Z.M., Richardson M.D., Coburn M.S. Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the inferior colliculus of the pallid bat. J. Neurophysiol. 2006, 96:1320-1336.
28. Gordon M., O'Neill W.E. Temporal processing across frequency channels by FM selective auditory neurons can account for FM rate selectivity. Hear. Res. 1998, 122:97-108.
29. Harris D.M., Dallos P. Forward masking of auditory-nerve fiber responses. J. Neurophysiol. 1979, 42:1083-1107.
30. Heil P., Rajan R., Irvine D.R.F. Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: Effects of variation of stimulus parameters. Hear. Res. 1992, 63:108-134.
31. Heil P., Irvine D.R.F. Functional specialization in auditory cortex: responses to frequency-modulated stimuli in the cat's posterior auditory field. J. Neurophysiol. 1998, 79:3041-3059.
32. Kaltenbach J.A., Meleca R.J., Falzarano P. Forward masking properties of neurons in the dorsal cochlear nucleus. Soc. Neurosci. Abstr. 1992, 18:149.
33. Kanwal J.S., Matsumura S., Ohlemiller K., Suga N. Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats. J. Acoust. Soc. Am. 1994, 96:1229-1254.
34. Klein D.J., Depireux D.A., Simon J.Z., Shamma S.A. Robust spectrotemporal reverse correlation for the auditory system: optimizing stimulus design. J. Comput. Neurosci. 2000, 9:85-111.
35. Kowalski N., Depireux D.A., Shamma S.A. Analysis of dynamic spectra in ferret primary auditory cortex. I. Characteristics of single-unit responses to moving ripple spectra. J. Neurophysiol. 1996, 76:3503-3523.
36. Kvale M.N., Schreiner C.E. Short-term adaptation of auditory receptive fields to dynamic stimuli. J. Neurophysiol. 2004, 91:604-612.
37. Leroy S.A., Wenstrup J.J. Spectral integration in the inferior colliculus of the mustached bat. J. Neurosci. 2000, 20:8533-8541.
38. Linden J.F., Liu R.C., Sahani M., Schreiner C.E., Merzenich M.M. Spectrotemporal structure of receptive fields in areas AI and AAF of mouse auditory cortex. J. Neurophysiol. 2003, 90:2660-2675.
39. Machens C.K., Wehr M.S., Zador A.M. Linearity of cortical receptive fields measured with natural sounds. J. Neurosci. 2004, 24:1089-1100.
40. Mendelson J.R., Cynader M.S. Sensitivity of cat primary auditory cortex (A1) neurons to the direction and rate of frequency modulation. Brain Res. 1985, 327:331-335.
41. Miller L.M., Escabi M.A., Read H.L., Schreiner C.E. Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J. Neurophysiol. 2002, 87:516-527.
42. Mittmann D.H., Wenstrup J.J. Combination-sensitive neurons in the inferior colliculus. Hear. Res. 1995, 90:185-191.
43. Nataraj K., Wenstrup J.J. Roles of inhibition in complex auditory responses in the inferior colliculus: inhibited combination-sensitive neurons. J. Neurophysiol. 2006, 95:2179-2192.
44. O'Neill W.E. The bat auditory cortex. Hearing by Bats 1995, 416-480. Springer-Verlag, New York. A.N. Popper, R.R. Fay (Eds.).
45. O'Neill W.E., Suga N. Target-range sensitive neurons in the auditory cortex of the mustached bat. Science 1979, 203:69-73.
46. Olsen J.F., Suga N. Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J. Neurophysiol. 1991, 65:1254-1274.
47. Peterson D.C., Voytenko S., Gans D., Galazyuk A., Wenstrup J.J. Intracellular recordings from combination-sensitive neurons in the inferior colliculus. J. Neurophysiol. 2008, 100:629-645.
48. Plack C.J., Oxenham A.J., Drga V. Masking by inaudible sounds and the linearity of temporal summation. J. Neurosci. 2006, 26:8767-8773.
49. Portfors C.V., Wenstrup J.J. Delay-tuned neurons in the inferior colliculus of the mustached bat: implications for analyses of target distance. J. Neurophysiol. 1999, 82:1326-1338.
50. Portfors C.V., Wenstrup J.J. Responses to combinations of tones in the nuclei of the lateral lemniscus. J. Assoc. Res. Otolaryngol. 2001, 2:104-117.
51. Portfors C.V., Wenstrup J.J. Excitatory and facilitatory frequency response areas in the inferior colliculus of the mustached bat. Hear. Res. 2002, 168:131-138.
52. Rall W.A. Theoretical significance of dendritic trees for neuronal input-output relations. Neural theory and modelling 1964, 73-97. Stanford University Press, Stanford, CA. R.F. Reiss (Ed.).
53. Rhode W.S., Greenberg S. Lateral suppression and inhibition in the cochlear nucleus of the cat. J. Neurophysiol. 1994, 71:493-514.
54. Rieke F., Bodnar D.A., Bialek W. Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc. Biol. Sci. 1995, 262:259-265.
55. Roverud R.C. Neural computations for sound pattern recognition: evidence for summation of an array of frequency filters in an echolocating bat. J. Neurosci. 1993, 13:2306-2312.
56. Rutkowski R.G., Shackleton T.M., Schnupp J.W., Wallace M.N., Palmer A.R. Spectrotemporal receptive field properties of single units in the primary, dorsocaudal and ventrorostral auditory cortex of the guinea pig. Audiol. Neurotol. 2002, 7:214-227.
57. Sanchez J.T., Gans D., Wenstrup J.J. Glycinergic " inhibition" mediates selective excitatory responses to combinations of sounds. J. Neurosci. 2008, 28:80-90.
58. Schuller G., Radtke-Schuller S., Betz M. A stereotaxic method for small animals using experimentally determined reference profiles. J. Neurosci. Methods 1986, 18:339-350.
59. Segev I., Rall W. Excitable dendrites and spines: earlier theoretical insights elucidate recent direct observations. Trends Neurosci. 1998, 21:453-460.
60. Sen K., Theunissen F.E., Doupe A.J. Feature analysis of natural sounds in the songbird auditory forebrain. J. Neurophysiol. 2001, 86:1445-1458.
61. Shannon-Hartman S., Wong D., Maekawa M. Processing of pure-tone and FM stimuli in the auditory cortex of the FM bat, Myotis lucifugus. Hear. Res. 1992, 61:179-188.
62. Shechter B., Depireux D.A. Stability of spectro-temporal tuning over several seconds in primary auditory cortex of the awake ferret. Neuroscience 2007, 148:806-814.
63. Singh N.C., Theunissen F.E. Modulation spectra of natural sounds and ethological theories of auditory processing. J. Acoust. Soc. Am. 2003, 114:3394-3411.
64. Suga N. Analysis of frequency-modulated sounds by auditory neurons of echo-locating bats. J. Physiol. 1965, 179:26-53.
65. Suga N., O'Neill W.E. Neural axis representing target range in the auditory cortex of the mustached bat. Science 1979, 206:351-353.
66. Suga N., O'Neill W.E., Kujirai K., Manabe T. Specificity of " combination sensitive" neurons for processing complex biosonar signals in the auditory cortex of the mustached bat. J. Neurophysiol. 1983, 49:1573-1626.
67. Suga N., O'Neill W.E., Manabe T. Cortical neurons sensitive to combinations of information-bearing elements of biosonar signals in the mustached bat. Science 1978, 200:778-781.
68. Suga N., Schlegel P. Coding and processing in the auditory systems of FM-signal-producing bats. J. Acoust. Soc. Am. 1973, 54:174-190.
69. Suga N., Simmons J.A., Shimozawa T. Neurophysiological studies on echolocation systems in awake bats producing CF-FM orientation sounds. J. Exp. Biol. 1974, 61:379-399.
70. Sutter M.L., Schreiner C.E., McLean M., O'Connor K.N., Loftus W.C. Organization of inhibitory frequency receptive fields in cat primary auditory cortex. J. Neurophysiol. 1999, 82:2358-2371.
71. Theunissen F.E., Sen K., Doupe A.J. Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J. Neurosci. 2000, 20:2315-2331.
72. Theunissen F.E., Woolley S.M., Hsu A., Fremouw T. Methods for the analysis of auditory processing in the brain. Ann. N.Y. Acad. Sci. 2004, 1016:187-207.
73. Valentine P.A., Eggermont J.J. Stimulus dependence of spectro-temporal receptive fields in cat primary auditory cortex. Hear. Res. 2004, 196:119-133.
74. Walton J.P., Frisina R.D., Ison J.R., O'Neill W.E. Neural correlates of behavioral gap detection in the inferior colliculus of the young CBA mouse. J. Compar. Physiol. A Sensory Neural Behav. Physiol. 1997, 181:161-176.
75. Warren S., Hamalainen H.A., Gardner E.P. Objective classification of motion- and direction-sensitive neurons in primary somatosensory cortex of awake monkeys. J. Neurophysiol. 1986, 56:598-622.
76. Wehr M., Zador A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426:442-446.
77. Westerman L.A., Smith R.L. Rapid and short-term adaptation in auditory nerve responses. Hear. Res. 1984, 15:249-260.
78. Wickesberg R.E., Oertel D. Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J. Neurosci. 1990, 10:1762-1768.
79. Woolley S.M., Gill P.R., Theunissen F.E. Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain. J. Neurosci. 2006, 26:2499-2512.