Two-dimensional adaptation in the auditory forebrain

Journal of Neurophysiology

Volumn 106, Issue 4, 2011, Pages 1841-1861

  Sharpee, Tatyana O ^a,b   Nagel, Katherine I ^b   Doupe, Allison J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Information theory; Neural coding; Receptive field; Spike triggered average; Spike triggered covariance

Indexed keywords

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; FOREBRAIN; NERVE POTENTIAL; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; SECONDARY AUDITORY CORTEX; SPIKE WAVE;

ACOUSTIC STIMULATION; ACOUSTICS; ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUDITORY CORTEX; BRAIN MAPPING; EVOKED POTENTIALS, AUDITORY; FINCHES; MODELS, NEUROLOGICAL; NEURONS; OSCILLOMETRY;

EID: 80054027328     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00905.2010     Document Type: Article

References (120)

1. Abramowitz M, Stegun IA. Handbook of Mathematical Functions. Washington, DC: US Government Printing Office, 1964.
2. Adelman TL, Bialek W, Olberg RM. The information content of receptive fields. Neuron 40: 823-833, 2003.
3. Agüera y Arcas B, Fairhall AL. What causes a neuron to spike? Neural Comput 15: 1789-1807, 2003.
4. Agüera y Arcas B, Fairhall AL, Bialek W. Computation in a single neuron: Hodgkin and Huxley revisited. Neural Comput 15: 1715-1749, 2003.
5. Aldworth ZN, Miller JP, Gedeon T, Cummins GI, Dimitrov AG. Dejittered spike-conditioned stimulus waveforms yield improved estimates of neuronal feature selectivity and spike-timing precision of sensory interneurons. J Neurosci 25: 5323-5332, 2005.
6. Atencio CA, Sharpee TO, Schreiner CE. Cooperative nonlinearities in auditory cortical neurons. Neuron 58: 956-966, 2008.
7. Atencio CA, Sharpee TO, Schreiner CE. Hierarchical computation in the canonical auditory cortical circuit. Proc Natl Acad Sci U S A 106: 21894- 21899, 2009.
8. Atick JJ, Redlich AN. What does the retina know about natural scenes? Neural Comput 4: 196-210, 1992.
9. Baccus SA, Meister M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36: 909-919, 2002.
10. Bair W. Spike timing in the mammalian visual system. Curr Opin Neurobiol 9: 447-453, 1999.
11. Bandyopadhyay S, Reiss LA, Young ED. Receptive field for dorsal cochlear nucleus neurons at multiple sound levels. J Neurophysiol 98: 3505-3515, 2007.
12. Bar-Yosef O, Nelken I. The effects of background noise on the neural responses to natural sounds in cat primary auditory cortex. Front Comput Neurosci 1: 3, 2007.
13. 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 22: 8619-8632, 2002.
14. Barlow HB. Possible principles underlying the transformation of sensory messages. In: Sensory Communication, edited by Rosenblith WA. Cambridge, MA: MIT, 1961, p. 217-234.
15. Barlow HB, Fitzhugh R, Kuffler SW. Change of organization in the receptive fields of the cat's retina during dark adaptation. J Physiol 137: 338-354, 1957.
16. Berry MJ, Warland DK, Meister M. The structure and precision of retinal spike trains. Proc Natl Acad Sci U S A 94: 5411-5416, 1997.
17. Bialek W, de Ruyter van Steveninck RR. Features and dimensions: motion estimation in fly vision (Online). http://arxiv.org/abs/q-bio/0505003.
18. Bialek W, Rieke F, de Ruyter van Steveninck RR, Warland D. Reading a neural code. Science 252: 1854-1857, 1991.
19. Borst A, Flanagin VL, Sompolinsky H. Adaptation without parameter change: Dynamic gain control in motion detection. Proc Natl Acad Sci U S A 102: 6172-6176, 2005.
20. Bracewell RN. The Fourier Transform and Its Applications. New York: McGraw-Hill, 1986.
21. Brenner N, Bialek W, de Ruyter van Steveninck R. Adaptive rescaling maximizes information transmission. Neuron 26: 695-702, 2000a.
22. Brenner N, Strong SP, Koberle R, Bialek W, de Ruyter van Steveninck RR. Synergy in a neural code. Neural Comput 12: 1531-1552, 2000b.
23. Bryant HL, Segundo JP. Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260: 279-314, 1976.
24. Chander D, Chichilnisky EJ. Adaptation to temporal contrast in primate and salamander retina. J Neurosci 21: 9904-9916, 2001.
25. Chen X, Han F, Poo MM, Dan Y. Excitatory and suppressive receptive field subunits in awake monkey primary visual cortex (V1). Proc Natl Acad Sci U S A 104: 19120-19125, 2007.
26. Christianson GB, Sahani M, Linden JF. The consequences of response nonlinearities for interpretation of spectrotemporal receptive fields. J Neurosci 28: 446-455, 2008.
27. de Boer E, Kuyper P. Triggered correlation. IEEE Trans Biomed Eng 15: 169-179, 1968.
28. de Ruyter van Steveninck RR, Bialek W. Real-time performance of a movement-sensitive neuron in the blowfly visual system: coding and information transfer in short spike sequences. Proc R Soc Lond B Biol Sci 234: 379-414, 1988.
29. Dean I, Harper NS, McAlpine D. Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8: 1684-1689, 2005.
30. Depireux DA, Simon JZ, Klein DJ, Shamma SA. Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. J Neurophysiol 85: 1220-1234, 2001.
31. Deweese M. Optimization principles for the neural code. Network 7: 325-331, 1996.
32. DeWeese MR, Wehr M, Zador AM. Binary spiking in auditory cortex. J Neurosci 23: 7940-7949, 2003.
33. Dimitrov AG, Gedeon T. Effects of stimulus transformations on estimates of sensory neuron selectivity. J Comput Neurosci 20: 265-283, 2006.
34. Dimitrov AG, Sheiko MA, Baker J, Yen SC. Spatial and temporal jitter distort estimated functional properties of visual sensory neurons. J Comput Neurosci 27: 309-319, 2009.
35. Eggermont JJ. Wiener and Volterra analyses applied to the auditory system. Hear Res 66: 177-201, 1993.
36. Eggermont JJ, Epping WJ, Aertsen AM. Stimulus dependent neural correlations in the auditory midbrain of the grassfrog (Rana temporaria L.). Biol Cybern 47: 103-117, 1983.
37. Enroth-Cugell C, Lennie P. The control of retinal ganglion cell discharge by receptive field surrounds. J Physiol 247: 551-578, 1975.
38. Epping WJ, Eggermont JJ. Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. II. Stimulation with amplitude modulated sound. Hear Res 24: 55-72, 1986.
39. Escabi MA, Miller LM, Read HL, Schreiner CE. Naturalistic auditory contrast improves spectrotemporal coding in the cat inferior colliculus. J Neurosci 23: 11489-11504, 2003.
40. Fairhall AL, Burlingame CA, Narasimhan R, Harris RA, Puchalla JL, Berry MJ 2nd. Selectivity for multiple stimulus features in retinal ganglion cells. J Neurophysiol 96: 2724-2738, 2006.
41. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR. Efficiency and ambiguity in an adaptive neural code. Nature 412: 787-792, 2001.
42. Fortune ES, Margoliash D. Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopygia guttata). J Comp Neurol 325: 388-404, 1992.
43. Fortune ES, Margoliash D. Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J Comp Neurol 360: 413-441, 1995.
44. Frisina RD, Smith RL, Chamberlain SC. Encoding of amplitude modulation in the gerbil cochlear nucleus. I. A hierarchy of enhancement. Hear Res 44: 99-122, 1990.
45. Galazyuk AV, Feng AS. Oscillation may play a role in time domain central auditory processing. J Neurosci 21: RC147, 2001.
46. Garcia-Lazaro JA, Ahmed B, Schnupp JW. Tuning to natural stimulus dynamics in primary auditory cortex. Curr Biol 16: 264-271, 2006.
47. Gill P, Woolley SM, Fremouw T, Theunissen FE. What's that sound? Auditory area CLM encodes stimulus surprise, not intensity or intensity changes. J Neurophysiol 99: 2809-2820, 2008.
48. Gill P, Zhang J, Woolley SM, Fremouw T, Theunissen FE. Sound representation methods for spectro-temporal receptive field estimation. J Comput Neurosci 21: 5-20, 2006.
49. Gollisch T. Estimating receptive fields in the presence of spike-time jitter. Network 17: 103-129, 2006.
50. Heil P, Irvine DR. First-spike timing of auditory-nerve fibers and comparison with auditory cortex. J Neurophysiol 78: 2438-2454, 1997.
51. Heil P, Irvine DR. On determinants of first-spike latency in auditory cortex. Neuroreport 7: 3073-3076, 1996.
52. Heil P, Irvine DR. The posterior field P of cat auditory cortex: coding of envelope transients. Cereb Cortex 8: 125-141, 1998.
53. Heil P, Neubauer H. Temporal integration of sound pressure determines thresholds of auditory-nerve fibers. J Neurosci 21: 7404-7415, 2001.
54. Heil P, Neubauer H. A unifying basis of auditory thresholds based on temporal summation. Proc Natl Acad Sci U S A 100: 6151-6156, 2003.
55. Heil P, Neubauer H, Brown M, Irvine DR. Towards a unifying basis of auditory thresholds: distributions of the first-spike latencies of auditorynerve fibers. Hear Res 238: 25-38, 2008.
56. Hong S, Aguera y Arcas B, Fairhall AL. Single neuron computation: from dynamical system to feature detector. Neural Comput 19: 3133-3172, 2007.
57. Hong S, Lundstrom BN, Fairhall AL. Intrinsic gain modulation and adaptive neural coding. PLoS Comput Biol 4: e1000119, 2008.
58. Hsu A, Woolley SM, Fremouw TE, Theunissen FE. Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons. J Neurosci 24: 9201-9211, 2004.
59. Jerri AJ. The Shannon sampling theorem-its various extensions and applications: a tutorial review. Proc IEEE Inst Electr Electron Eng 65: 1565-1596, 1977.
60. Kim AJ, Lazar AA, Slutskiy YB. System identification of Drosophila olfactory sensory neurons. J Comput Neurosci 30: 143-161, 2011.
61. Kim PJ, Young ED. Comparative analysis of spectro-temporal receptive fields, reverse correlation functions, and frequency tuning curves of auditory- nerve fibers. J Acoust Soc Am 95: 410-422, 1994.
62. Klein DJ, Depireux DA, Simon JZ, Shamma SA. Robust spectrotemporal reverse correlation for the auditory system: optimizing stimulus design. J Comput Neurosci 9: 85-111, 2000.
63. Klein DJ, Simon JZ, Depireux DA, Shamma SA. Stimulus-invariant processing and spectrotemporal reverse correlation in primary auditory cortex. J Comput Neurosci 20: 111-136, 2006.
64. Kouh M, Sharpee TO. Estimating linear-nonlinear models using Renyi divergences. Network 20: 49-68, 2009.
65. Krishna BS, Semple MN. Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J Neurophysiol 84: 255-273, 2000.
66. Kuffler SW, Fitzhugh R, Barlow HB. Maintained activity in the cat's retina in light and darkness. J Gen Physiol 40: 683-702, 1957.
67. Kvale MN, Schreiner CE. Short-term adaptation of auditory receptive fields to dynamic stimuli. J Neurophysiol 91: 604-612, 2004.
68. Lesica NA, Grothe B. Dynamic spectrotemporal feature selectivity in the auditory midbrain. J Neurosci 28: 5412-5421, 2008a.
69. Lesica NA, Grothe B. Efficient temporal processing of naturalistic sounds. PLos One 3: e1655, 2008b.
70. Lewicki MS. Efficient coding of natural sounds. Nat Neurosci 5: 356-363, 2002.
71. Machens CK, Wehr MS, Zador AM. Linearity of cortical receptive fields measured with natural sounds. J Neurosci 24: 1089-1100, 2004.
72. Mainen ZF, Sejnowski TJ. Reliability of spike timing in neocortical neurons. Science 268: 1503-1506, 1995.
73. Malone BJ, Scott BH, Semple MN. Dynamic amplitude coding in the auditory cortex of awake rhesus macaques. J Neurophysiol 98: 1451-1474, 2007.
74. Maravall M, Petersen RS, Fairhall AL, Arabzadeh E, Diamond ME. Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biol 5: e19, 2007.
75. Meister M, Berry MJ. The neural code of the retina. Neuron 22: 435-450, 1999.
76. Nagel K, Doupe AJ. Temporal processing and adaptation in the songbird auditory forebrain. Neuron 51: 845-859, 2006.
77. Nagel KI, Doupe AJ. Organizing principles of spectro-temporal encoding in the avian primary auditory area field L. Neuron 58: 938-955, 2008.
78. Nelken I, Chechik G. Information theory in auditory research. Hear Res 229: 94-105, 2007.
79. Nelken I, Kim PJ, Young ED. Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. II. Predicting responses with the use of nonlinear models. J Neurophysiol 78: 800-811, 1997.
80. Nelken I, Rotman Y, Bar Yosef O. Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397: 154-157, 1999.
81. Paninski L. Convergence properties of three spike-triggered analysis techniques. Network 14: 437-464, 2003.
82. Petersen CC. The functional organization of the barrel cortex. Neuron 56: 339-355, 2007.
83. Phillips CG, Zeki S, Barlow HB. Localization of function in the cerebral cortex. Past, present and future. Brain 107: 327-361, 1984.
84. Pillow JW, Simoncelli EP. Dimensionality reduction in neural models: an information-theoretic generalization of spike-triggered average and covariance analysis. J Vis 6: 414-428, 2006.
85. Prenger R, Wu MC, David SV, Gallant JL. Nonlinear V1 responses to natural scenes revealed by neural network analysis. Neural Netw 17: 663-679, 2004.
86. Rees A, Moller AR. Stimulus properties influencing the responses of inferior colliculus neurons to amplitude-modulated sounds. Hear Res 27: 129-143, 1987.
87. Reiss LA, Bandyopadhyay S, Young ED. Effects of stimulus spectral contrast on receptive fields of dorsal cochlear nucleus neurons. J Neurophysiol 98: 2133-2143, 2007.
88. Rieke F, Warland D, de Ruyter van Steveninck R, Bialek WB. Spikes: Exploring the Neural Code. Cambridge, MA: MIT, 1997.
89. Rowekamp RJ, Sharpee TO. Analyzing multicomponent receptive fields from neural responses to natural stimuli. Network. doi:10.3109/ 0954898x.2011.566303.
90. Ruderman DL, Bialek W. Statistics of natural images: scaling in the woods. Phys Rev Lett 73: 814-817, 1994.
91. Rust NC, Schwartz O, Movshon JA, Simoncelli EP. Spatiotemporal elements of macaque v1 receptive fields. Neuron 46: 945-956, 2005.
92. Schwartz O, Pillow JW, Rust NC, Simoncelli EP. Spike-triggered neural characterization. J Vis 6: 484-507, 2006.
93. Scott BH, Malone BJ, Semple MN. Transformation of temporal processing across auditory cortex of awake macaques. J Neurophysiol 105: 712-730, 2011.
94. Shannon CE. Communication in the presence of noise. Proceedings of the IRE 37: 10-21, 1949.
95. Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M. Speech recognition with primarily temporal cues. Science 270: 303-304, 1995.
96. Shapley RM, Enroth-Cugell C. Visual adaptation and retinal gain controls. Prog Retin Eye Res 3: 263-346, 1984.
97. Shapley RM, Victor JD. The effect of contrast on the transfer properties of cat retinal ganglion cells. J Physiol 285: 275-298, 1978.
98. Sharpee T, Rust NC, Bialek W. Analyzing neural responses to natural signals: maximally informative dimensions. Neural Comput 16: 223-250, 2004.
99. Sharpee TO, Sugihara H, Kurgansky AV, Rebrik SP, Stryker MP, Miller KD. Adaptive filtering enhances information transmission in visual cortex. Nature 439: 936-942, 2006.
100. Singh NC, Theunissen FE. Modulation spectra of natural sounds and ethological theories of auditory processing. J Acoust Soc Am 114: 3394-3411, 2003.
101. Slee SJ, Higgs MH, Fairhall AL, Spain WJ. Two-dimensional time coding in the auditory brainstem. J Neurosci 25: 9978-9988, 2005.
102. Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386: 69-73, 1997.
103. Srinivasan MV, Laughlin SB, Dubs A. Predictive coding: a fresh view of inhibition in the retina. Proc R Soc Lond B Biol Sci B216: 427-459, 1982.
104. Strong SP, Koberle R, de Ruyter van Steveninck RR, Bialek W. Entropy and information in neural spike trains. Phys Rev Lett 80: 197-200, 1998.
105. Sullivan WE 3rd. Possible neural mechanisms of target distance coding in auditory system of the echolocating bat Myotis lucifugus. J Neurophysiol 48: 1033-1047, 1982.
106. Teich MC, Heneghan C, Lowen SB, Ozaki T, Kaplan E. Fractal character of the neural spike train in the visual system of the cat. J Opt Soc Am A Opt Image Sci Vis 14: 529-546, 1997.
107. Theunissen FE, David SV, Singh NC, Hsu A, Vinje WE, Gallant JL. Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network 12: 289-316, 2001.
108. Theunissen FE, Doupe AJ. Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches. J Neurosci 18: 3786-3802, 1998.
109. Theunissen FE, Sen K, Doupe AJ. Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J Neurosci 20: 2315-2331, 2000.
110. Tiesinga P, Fellous JM, Sejnowski TJ. Regulation of spike timing in visual cortical circuits. Nat Rev Neurosci 9: 97-107, 2008.
111. Touryan J, Felsen G, Dan Y. Spatial structure of complex cell receptive fields measured with natural images. Neuron 45: 781-791, 2005.
112. Touryan J, Lau B, Dan Y. Isolation of relevant visual features from random stimuli for cortical complex cells. J Neurosci 22: 10811-10818, 2002.
113. Treves A, Panzeri S. The upward bias in measures of information derived from limited data samples. Neural Comput 7: 399-407, 1995.
114. Victor JD. The dynamics of the cat retinal x-cell centre. J Physiol 386: 219-246, 1987.
115. Victor JD, Mechler F, Repucci MA, Purpura KP, Sharpee T. Responses of V1 neurons to two-dimensional hermite functions. J Neurophysiol 95: 379-400, 2006.
116. Voss RF, Clarke J. "1/f noise" in music and speech. Nature 258: 317-318, 1975.
117. Wiener N. Extrapolation, Interpolation, and Smoothing of Stationary Time Series: With Engineering Applications. Cambridge, MA: MIT, 1964.
118. Wild JM, Karten HJ, Frost BJ. Connections of the auditory forebrain in the pigeon (Columba livia). J Comp Neurol 337: 32-62, 1993.
119. Woolley SM, Gill PR, Theunissen FE. Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain. J Neurosci 26: 2499-2512, 2006.
120. Zhou Y, Wang X. Cortical processing of dynamic sound envelope transitions. J Neurosci 30: 16741-16754, 2010.