Complex spectral interactions encoded by auditory cortical neurons: Relationship between bandwidth and pattern

Frontiers in Systems Neuroscience

Volumn 4, Issue , 2010, Pages

  O'Connor, Kevin N ^a,b   Yin, Pingbo ^a,c   Petkov, Christopher I ^a,d   Sutter, Mitchell L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Auditory cortex; Ripple; Spectral Gabor; Spectral interactions

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY CORTEX NEURON; AUDITORY STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CONTROLLED STUDY; FEMALE; HISTOLOGY; MALE; NONHUMAN; RHESUS MONKEY; STATISTICAL MODEL; STIMULUS RESPONSE; SYSTEMS BIOLOGY;

EID: 79957903950     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2010.00145     Document Type: Article

References (95)

1. Abeles, M., and Goldstein, M. H. Jr. (1970). Functional architecture in cat primary auditory cortex: columnar organization and organization according to depth. J. Neurophysiol. 33, 172-187.
2. Ahmed, B., Garcia-Lazaro, J. A., and Schnupp, J. W. (2006). Response linearity in primary auditory cortex of the ferret. J. Physiol. 572, 763-773.
3. Atencio, C.A., Sharpee, T. O., and Schreiner, C. E. (2008). Cooperative nonlinearities in auditory cortical neurons. Neuron 58, 956-966.
4. Barbour, D. L., and Wang, X. (2002). Temporal coherence sensitivity in auditory cortex. J. Neurophysiol. 88, 2684-2699.
5. Barbour, D. L., and Wang, X. (2003). Auditory cortical responses elicited in awake primates by random spectrum stimuli. J. Neurosci. 23, 7194-7206.
6. Bar-Yosef, O., Rotman, Y., and Nelken, I. (2002). Responses of neurons in cat primary auditory cortex to bird chirps, effects of temporal and spectral context. J. Neurosci. 22, 8619-8632.
7. Bieser, A., and Muller-Preuss, P. (1996). Auditory responsive cortex in the squirrel monkey, neural responses to amplitude-modulated sounds. Exp. Brain Res. 108, 273-284.
8. Bizley, J. K., Walker, K. M., Silverman, B. W., King, A. J., and Schnupp, J. W. (2009). Interdependent encoding of pitch, timbre, and spatial location in auditory cortex. J. Neurosci. 29, 2064-2075.
9. Bleeck, S., Patterson, R. D., and Winter, I. M. (2003). Using genetic algorithms to find the most effective stimulus for sensory neurons. J. Neurosci. Methods 125, 73-82.
10. Bradbury, J. W., and Vehrencamp, S. L. (1998). The Principles of Animal Communication. Sunderland, MA: Sinauer Associates.
11. Brosch, M., and Schreiner, C. E. (2000). Sequence sensitivity of neurons in cat primary auditory cortex. Cereb. Cortex 10, 1155-1167.
12. Brosch, M., Schulz, A., and Scheich, H. (1999). Processing of sound sequences in macaque auditory cortex: response enhancement. J. Neurophysiol. 82, 1542-1559.
13. Cadieu, C., Kouh, M., Pasupathy, A., Connor, C. E., Riesenhuber, M., and Poggio, T. (2007). A model of V4 shape selectivity and invariance. J. Neurophysiol. 98, 1733-1750.
14. Calhoun, B. M., and Schreiner, C. E. (1998). Spectral envelope coding in cat primary auditory cortex: linear and non-linear effects of stimulus characteristics. Eur. J. Neurosci. 10, 926-940.
15. Creutzfeldt, O., Hellweg, F. C., and Schreiner, C. (1980). Thalamocortical transformation of responses to complex auditory stimuli. Exp. Brain Res. 39, 87-104.
16. deCharms, R. C., Blake, D. T., and Merzenich, M. M. (1998). Optimizing sound features for cortical neurons. Science 280, 1439-1443.
17. DiMattina, C., and Wang, X. (2006). Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations. J. Neurophysiol. 95, 1244-1262.
18. Efron, B., and Tibshirani, R. J. (1993). An Introduction to the Bootstrap. New York, NY: Chapman & Hall.
19. Eggermont, J. J. (1994). Temporal modulation transfer functions for AM and FM stimuli in cat auditory cortex. Effects of carrier type, modulating waveform and intensity. Hear. Res. 74, 51-66.
20. Fant, G. (1973). Speech Sounds and Features. Cambridge, MA: MIT Press.
21. Finlayson, P. G. (1999). Post-stimulatory suppression, facilitation and tuning for delays shape responses of inferior colliculus neurons to sequential pure tones. Hear. Res. 131, 177-194.
22. Firzlaff, U., Schuchmann, M., Grunwald, J. E., Schuller, G., and Wiegrebe, L. (2007). Object-oriented echo perception and cortical representation in echolocating bats. PLoS Biol. 5, e100. doi: 10.1371/journal.pbio.0050100.
23. Firzlaff, U., and Schuller, G. (2007). Cortical responses to object size- dependent spectral interference patterns in echolocating bats. Eur. J. Neurosci. 26, 2747-2755.
24. Fishbach, A., Nelken, I., and Yeshurun, Y. (2001). Auditory edge detection: a neural model for physiological and psychoacoustical responses to amplitude transients. J. Neurophysiol. 85, 2303-2323.
25. Fitzpatrick, D. C., Kanwal, J. S., Butman, J. A., and Suga, N. (1993). Combinationsensitive neurons in the primary auditory cortex of the mustached bat. J. Neurosci. 13, 931-940.
26. Fukushima, K., Miyake, S., and Ito, T. (1983). Neocognitron: a self-organizing network model for a mechanism of visual pattern recognition. IEEE Trans. Syst. Man Cybern. 13, 826-834.
27. Gaese, B. H., and Ostwald, J. (1995). Temporal coding of amplitude and frequency modulation in the rat auditory cortex. Eur. J. Neurosci. 7, 438-450.
28. Gawne, T. J., Richmond, B. J., and Optican, L. M. (1991). Interactive effects among several stimulus parameters on the responses of striate cortical complex cells. J. Neurophysiol. 66, 379-389.
29. Geman, S. (2006). Invariance and selectivity in the ventral visual pathway. J. Physiol. (Paris) 100, 212-224.
30. Gourevitch, B., and Eggermont, J. J. (2007). Spatial representation of neural responses to natural and altered conspecific vocalizations in cat auditory cortex. J. Neurophysiol. 97, 144-158.
31. Gourevitch, B., Norena, A., Shaw, G., and Eggermont, J. J. (2009). Spectrotemporal receptive fields in anesthetized cat primary auditory cortex are context dependent. Cereb. Cortex 19, 1448-1461.
32. Grossberg, S. (1973). Contour enhancement, short term memory, and constancies in reverberating neural networks. Stud. Appl. Math. 52, 213-257.
33. Hays, W. L. (1988). Statistics. New York: Holt Rinehart and Winston.
34. Heil, P., and Irvine, D. R. (1998). Functional specialization in auditory cortex: responses to frequency-modulated stimuli in the cat's posterior auditory field. J. Neurophysiol. 79, 3041-3059.
35. Hromadka, T., Deweese, M. R., and Zador, A. M. (2008). Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 6, e16. doi: 10.1371/ journal.pbio.0060016.
36. Hubel, D. H., and Wiesel, T. N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106-154.
37. Ison, M. J., and Quiroga, R. Q. (2008). Selectivity and invariance for visual object perception. Front. Biosci. 13, 4889-4903.
38. Kadia, S. C., and Wang, X. (2003). Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. J. Neurophysiol. 89, 1603-1622.
39. Kaur, S., Lazar, R., and Metherate, R. (2004). Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J. Neurophysiol. 91, 2551-2567.
40. Kaur, S., Rose, H. J., Lazar, R., Liang, K., and Metherate, R. (2005). Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivo and in vitro. Neuroscience 134, 1033-1045.
41. Klein, D. J., Simon, J. Z., Depireux, D. A., and Shamma, S. A. (2006). Stimulusinvariant processing and spectrotemporal reverse correlation in primary auditory cortex. J. Comput. Neurosci. 20, 111-136.
42. Kouh, M., and Poggio, T. (2008). A canonical neural circuit for cortical nonlinear operations. Neural Comput. 20, 1427-1451.
43. Kowalski, N., Depireux, D. A., and Shamma, S. A. (1996). Analysis of dynamic spectra in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary dynamic spectra. J. Neurophysiol. 76, 3524-3534.
44. Lu, T., Liang, L., and Wang, X. (2001). Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates. J. Neurophysiol. 85, 2364-2380.
45. Machens, C. K., Wehr, M. S., and Zador, A. M. (2004). Linearity of cortical receptive fields measured with natural sounds. J. Neurosci. 24, 1089-1100.
46. McKenna, T. M., Weinberger, N. M., and Diamond, D. M. (1989). Responses of single auditory cortical neurons to tone sequences. Brain Res. 481, 142-153.
47. Mendelson, J. R., Schreiner, C. E., Sutter, M. L., and Grasse, K. L. (1993). Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps. Exp. Brain Res. 94, 65-87.
48. Misawa, H., and Suga, N. (2001). Multiple combination-sensitive neurons in the auditory cortex of the mustached bat. Hear. Res. 151, 15-29.
49. Mittmann, D. H., and Wenstrup, J. J. (1995). Combination-sensitive neurons in the inferior colliculus. Hear. Res. 90, 185-191.
50. Morton, E. S. (1977). On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am. Nat. 111, 855-869.
51. Nelder, J.A. and Mead, R. (1965). A simplex method for function minimization. Comput. J. 7, 308-313.
52. Nelken, I., Prut, Y., Vaadia, E., and Abeles, M. (1994a). In search of the best stimulus: an optimization procedure for finding efficient stimuli in the cat auditory cortex. Hear. Res. 72, 237-253.
53. Nelken, I., Prut, Y., Vaddia, E., and Abeles, M. (1994b). Population responses to multifrequency sounds in the cat auditory cortex: four-tone complexes. Hear. Res. 72, 223-236.
54. Nelken, I., Rotman, Y., and Bar Yosef, O. (1999). Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397, 154-157.
55. O'Connor, K. N., Petkov, C. I., and Sutter, M. L. (2005). Adaptive stimulus optimization for auditory cortical neurons. J. Neurophysiol. 94, 4051-4067.
56. O'Neill, W. E., and Suga, N. (1982). Encoding of target range and its representation in the auditory cortex of the mustached bat. J. Neurosci. 2, 17-31.
57. Olsen, J. F., and Suga, N. (1991). Combination-sensitive neurons in the medial geniculate body of themustached bat: encoding of target range information. J. Neurophysiol. 65, 1275-1296.
58. Oonishi, S., and Katsuki, Y. (1965). Functional organization of and integrative mechanism on the auditory cortex of the cat. Jpn. J. Physol. 15.
59. Pandya, P. K., Rathbun, D. L., Moucha, R., Engineer, N. D., and Kilgard, M. P. (2008). Spectral and temporal processing in rat posterior auditory cortex. Cereb. Cortex 18, 301-314.
60. Paschal, W. G., and Wong, D. (1994). Frequency organization of delaysensitive neurons in the auditory cortex of the FM bat, Myotis lucifugus. J. Neurophysiol. 72, 366-379.
61. Petkov, C. I., O'Connor, K. N., and Sutter, M. L. (2007). Encoding of illusory continuity in primary auditory cortex. Neuron 54, 153-165.
62. Pienkowski, M., Shaw, G., and Eggermont, J. J. (2009). Wiener-Volterra characterization of neurons in primary auditory cortex using poisson-distributed impulse train inputs. J. Neurophysiol. 101, 3031-3041.
63. Portfors, C. V., and Felix, R. A. II. (2005). Spectral integration in the inferior colliculus of the CBA/CaJ mouse. Neuroscience 136, 1159-1170.
64. Press, W. H. (2000). Numerical Recipes in C the Art of Scientific Computing. Cambridge, England/New York/Los Alamos, CA: Cambridge University Press [distributed by] Los Alamos National Laboratory.
65. Qin, L., Sakai, M., Chimoto, S., and Sato, Y. (2004). Spectral-edge sensitivity of primary auditory cortex neurons in alert cats. Brain Res. 1014, 1-13.
66. Qiu, A., Schreiner, C. E., and Escabi, M. A. (2003). Gabor analysis of auditory midbrain receptive fields: spectrotemporal and binaural composition. J. Neurophysiol. 90, 456-476.
67. Rauschecker, J. P., and Tian, B. (2004). Processing of band-passed noise in the lateral auditory belt cortex of the rhesus monkey. J. Neurophysiol. 91, 2578-2589.
68. Recanzone, G. H. (2000). Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys. Hear. Res. 150, 104-118.
69. Riesenhuber, M., and Poggio, T. (1999). Hierarchical models of object recognition in cortex. Nat. Neurosci. 2, 1019-1025.
70. Rotman, Y., Bar-Yosef, O., and Nelken, I. (2001). Relating cluster and population responses to natural sounds and tonal stimuli in cat primary auditory cortex. Hear. Res. 152, 110-127.
71. Sadagopan, S., and Wang, X. (2009). Nonlinear spectrotemporal interactions underlying selectivity for complex sounds in auditory cortex. J. Neurosci. 29, 11192-11202.
72. Schebesch, G., Lingner, A., Firzlaff, U., Wiegrebe, L., and Grothe, B. (2010). Perception and neural representation of size-variant human vowels in the Mongolian gerbil (Meriones unguiculatus). Hear. Res. 261, 1-8.
73. Schnupp, J. W., Hall, T. M., Kokelaar, R. F., and Ahmed, B. (2006). Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J. Neurosci. 26, 4785-4795.
74. Schreiner, C. E., and Calhoun, B. M. (1994). Spectral envelope coding in cat primary auditory cortex: properties of ripple transfer functions. Aud. Neurosci. 1, 39-61.
75. Schreiner, C. E., and Urbas, J. V. (1986). Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF). Hear. Res. 21, 227-241.
76. Schuller, G., O'Neill, W. E., and Radtke- Schuller, S. (1991). Facilitation and delay sensitivity of auditory cortex neurons in CF-FM bats, Rhinolophus rouxi and Pteronotus p. parnellii. Eur. J. Neurosci. 3, 1165-1181.
77. Schulze, H., and G. Langner. (1999). Auditory cortical responses to amplitude modulations with spectra above frequency receptive fields: evidence for wide spectral integration. J. Comp. Physiol. A 185, 493-508.
78. Schwarz, D. W., and Tomlinson, R. W. (1990). Spectral response patterns of auditory cortex neurons to harmonic complex tones in alert monkey (Macaca mulatta). J. Neurophysiol. 64, 282-298.
79. Shamma, S. A., and Versnel, H. (1995). Ripple analysis in ferret primaryauditory cortex. II. Prediction of unit responses to arbitrary spectral profiles. Aud. Neurosci. 1, 255-270.
80. Shamma, S. A., Versnel, H., and Kowalski, N. (1995). Ripple analysis in ferret primary auditory cortex. I. Response characteristics of single units to sinusoidally rippled spectra. Aud. Neurosci. 1, 233-254.
81. Suga, N., and Manabe, T. (1982). Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J. Neurophysiol. 47, 225-255.
82. Suga, N., O'Neill, W. E., and Manabe, T. (1978). Cortical neurons sensitive to combinations of information-bearing elements of biosonar signals in the mustache bat. Science 200, 778-781.
83. Suga, N., O'Neill, W. E., and Manabe, T. (1979). Harmonic-sensitive neurons in the auditory cortex of the mustache bat. Science 203, 270-274.
84. Suga, N., and Tsuzuki, K. (1985). Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat. J. Neurophysiol. 53, 1109-1145.
85. Supin, A., Popov, V. V., Milekhina, O. N., and Tarakanov, M. B. (1999). Ripple depth and density resolution of rippled noise. J. Acoust. Soc. Am. 106, 2800-2804.
86. Supin, A. Y., Popov, V. V., Milekhina, O. N., and Tarakanov, M. B. (2003). Rippledspectrum resolution dependence on level. Hear. Res. 185, 1-12.
87. Sutter, M. L., and Schreiner, C. E. (1991). Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J. Neurophysiol. 65, 1207-1226.
88. Sutter, M. L., Schreiner, C. E., McLean, M., O'Connor, K. N., and Loftus, W. C. (1999). Organization of inhibitory frequency receptive fields in cat primary auditory cortex. J. Neurophysiol. 82, 2358-2371.
89. Theunissen, F. E., Sen, K., and Doupe, A. J. (2000). Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J. Neurosci. 20, 2315-2331.
90. Tsuzuki, K., and Suga, N. (1988). Combination-sensitive neurons in the ventroanterior area of theauditory cortex of the mustached bat. J. Neurophysiol. 60, 1908-1923.
91. Wang, X., and Kadia, S. C. (2001). Differential representation of speciesspecific primate vocalizations in the auditory cortices of marmoset and cat. J. Neurophysiol. 86, 2616-2620.
92. Wang, X., Merzenich, M. M., Beitel, R., and Schreiner, C. E. (1995). Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J. Neurophysiol. 74, 2685-2706.
93. Winter, I. M., and Palmer, A. R. (1995). Level dependence of cochlear nucleus onset unit responses and facilitation by second tones or broadband noise. J. Neurophysiol. 73, 141-159.
94. Winter, P., and Funkenstein, H. H. (1973). The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey (Saimiri sciureus). Exp. Brain Res. 18, 489-504.
95. Yu, J. J., and Young, E. D. (2000). Linear and nonlinear pathways of spectral information transmission in the cochlear nucleus. Proc. Natl. Acad. Sci. U.S.A. 97, 11780-11786.