Long-lasting context dependence constrains neural encoding models in rodent auditory cortex

Journal of Neurophysiology

Volumn 102, Issue 5, 2009, Pages 2638-2656

  Asari, Hiroki ^a,b   Zador, Anthony M ^a  

^a Watson School of Biological Sciences ^*  (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY THRESHOLD; BRAIN CELL; CONTROLLED STUDY; INTRACELLULAR RECORDING; MATHEMATICAL MODEL; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; THALAMUS;

ACOUSTIC STIMULATION; ANIMALS; ANIMALS, NEWBORN; AUDITORY CORTEX; AUDITORY PATHWAYS; AUDITORY PERCEPTION; COMPUTER SIMULATION; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, LONG-EVANS; SOUND; STATISTICS AS TOPIC; THALAMUS; TIME FACTORS;

EID: 70449366397     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00577.2009     Document Type: Article

References (72)

1. Abbott LF, Varela JA, Sen K, Nelson SB. Synaptic depression and cortical gain control. Science 275: 220-224, 1997. (Pubitemid 27034764)
2. Abeles M, Goldstein MH. Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs. Brain Res 42: 337-352, 1972.
3. Ahrens MB, Linden JF, Sahani M. Nonlinearities and contextual influences in auditory cortical responses modeled with multilinear spectrotemporal methods. J Neurosci 28: 1929-1942, 2008.
4. Baccus SA, Meister M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36: 909-919, 2002. (Pubitemid 35447862)
5. Barry PH. JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J Neurosci Methods 51: 107-116, 1994.
6. Bartlett EL, Wang X. Long-lasting modulation by stimulus context in primate auditory cortex. J Neurophysiol 94: 83-104, 2005. (Pubitemid 40923230)
7. 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. (Pubitemid 35387602)
8. Bregman AS. Auditory Scene Analysis: The Perceptual Organization of Sound. Cambridge, MA: MIT Press, 1994.
9. Brenner N, Bialek W, de Ruyter van Steveninck R. Adaptive rescaling maximizes information transmission. Neuron 26: 695-702, 2000. (Pubitemid 30953910)
10. Brosch M, Schreiner C. Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol 77: 923-943, 1997. (Pubitemid 27087789)
11. Brosch M, Schreiner C. Sequence sensitivity of neurons in cat primary auditory cortex. Cereb Cortex 10: 1155-1167, 2000. (Pubitemid 30954303)
12. Calford MB, Semple MN. Monaural inhibition in cat auditory cortex. J Neurophysiol 73: 1876-1891, 1995.
13. Carandini M, Ferster D. A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276: 949-952, 1997. (Pubitemid 27209093)
14. Carnevale NT, Johnston D. Electrophysiological characterization of remote chemical synapses. J Neurophysiol 47: 606-621, 1982.
15. Chichilnisky EJ. A simple white noise analysis of neuronal light responses. Network 12: 199-213, 2001.
16. Cleveland WS. Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74: 829-836, 1979.
17. Cleveland WS, Devlin SJ. Locally weighted regression: an approach to regression analysis by local fitting. J Am Stat Assoc 83: 596-610, 1988.
18. Cohen L. Time-Frequency Analysis. Englewood Cliffs, NJ: Prentice Hall, 1995.
19. Creutzfeldt O, Hellweg FC, Schreiner C. Thalamocortical transformation of responses to complex auditory stimuli. Exp Brain Res 39: 87-104, 1980. (Pubitemid 10122722)
20. David SV, Mesgarani N, Fritz JB, Shamma SA. Rapid synaptic depression explains nonlinear modulation of spectro-temporal tuning in primary auditory cortex by natural stimuli. J Neurosci 29: 3374-3386, 2009.
21. Dean I, Harper NS, McAlpine D. Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8: 1684-1689, 2005. (Pubitemid 41683195)
22. 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.
23. DeWeese MR, Zador AM. Asymmetric dynamics in optimal variance adaptation. Neural Comput 10: 1179-1202, 1998.
24. Eggermont JJ, Johannesma PM, Aertsen AM. Reverse-correlation methods in auditory research. Q Rev Biophys 16: 341-414, 1983.
25. Escabí MA, Schreiner CE. Nonlinear spectrotemporal sound analysis by neurons in the auditory midbrain. J Neurosci 22: 4114-4131, 2002.
26. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR. Efficiency and ambiguity in an adaptive neural code. Nature 412: 787-792, 2001. (Pubitemid 32801454)
27. Fishbach A, Nelken I, Yeshurun Y. Auditory edge detection: a neural model for physiological and psychoacoustical responses to amplitude transients. J Neurophysiol 85: 2303-2323, 2001. (Pubitemid 32525510)
28. Fishbach A, Yeshurun Y, Nelken I. Neural model for physiological responses to frequency and amplitude transitions uncovers topographical order in the auditory cortex. J Neurophysiol 90: 3663-3678, 2003. (Pubitemid 37541901)
29. Fritz J, Elhilali M, Shamma S. Active listening: task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex. Hear Res 206: 159-176, 2005. (Pubitemid 41085810)
30. Fritz J, Shamma S, Elhilali M, Klein D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci 6: 1216-1223, 2003. (Pubitemid 37346043)
31. Garcia-Lazaro JA, Ahmed B, Schnupp JWH. Tuning to natural stimulus dynamics in primary auditory cortex. Curr Biol 16: 264-271, 2006. (Pubitemid 43190225)
32. Gill P, Zhang J, Woolley SMN, Fremouw T, Theunissen FE. Sound representation methods for spectro-temporal receptive field estimation. J Comput Neurosci 21: 5-20, 2006. (Pubitemid 44028467)
33. Glucksberg S, Cowen GN. Memory for nonattended auditory material. Cogn Psychol 1: 149-156, 1970.
34. Hastie T, Tibshirani R, Friedman J. The Elements of Statistical Learning Theory. New York: Springer, 2001.
35. Hocherman S, Gilat E. Dependence of auditory cortex evoked unit activity on interstimulus interval in the cat. J Neurophysiol 45: 987-997, 1981. (Pubitemid 11078962)
36. Hromádka T, DeWeese MR, Zador AM. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 6: e16, 2008. (Pubitemid 351226052)
37. Joris PX, Schreiner CE, Rees A. Neural processing of amplitude-modulated sounds. Physiol Rev 84: 541-577, 2004.
38. 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.
39. Koch C, Poggio T, Torre V. Retinal ganglion cells: a functional interpretation of dendritic morphology. Philos Trans R Soc Lond B Biol Sci 298: 227-263, 1982.
40. Kowalski N, Depireux DA, Shamma SA. Analysis of dynamic spectra in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary dynamic spectra. J Neurophysiol 76: 3524-3534, 1996. (Pubitemid 26378118)
41. Kruskal WH, Wallis WA. Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47: 583-621, 1952.
42. Kubovy M, Howard FP. Persistence of pitch-segregating echoic memory. J Exp Psychol 2: 531-537, 1976.
43. Kvale MN, Schreiner CE. Short-term adaptation of auditory receptive fields to dynamic stimuli. J Neurophysiol 91: 604-612, 2004.
44. Linden JF, Liu RC, Sahani M, Schreiner CE, Merzenich MM. Spectrotemporal structure of receptive fields in areas AI and AAF of mouse auditory cortex. J Neurophysiol 90: 2660-2675, 2003. (Pubitemid 37266531)
45. Machens CK, Wehr MS, Zador AM. Linearity of cortical receptive fields measured with natural sounds. J Neurosci 24: 1089-1100, 2004.
46. Miller LM, Escabí MA, Read HL, Schreiner CE. Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J Neurophysiol 87: 516-527, 2002.
47. Monier C, Fournier J, Frégnac Y. In vitro and in vivo measures of evoked excitatory and inhibitory conductance dynamics in sensory cortices. J Neurosci Methods 169: 323-365, 2008.
48. Movshon JA, Lennie P. Pattern-selective adaptation in visual cortical neurons. Nature 278: 850-852, 1979. (Pubitemid 9148975)
49. Müller JR, Metha AB, Krauskopf J, Lennie P. Rapid adaptation in visual cortex to the structure of images. Science 285: 1405-1408, 1999. (Pubitemid 29411673)
50. Neisser U. Cognitive Psychology. New York: Meredith, 1967.
51. Nelken I, Fishbach A, Las L, Ulanovsky N, Farkas D. Primary auditory cortex of cats: feature detection or something else? Biol Cybern 89: 397-406, 2003.
52. Paninski L. Convergence properties of three spike-triggered analysis techniques. Network 14: 437-464, 2003. (Pubitemid 38011144)
53. Phillips DP. Temporal response features of cat auditory cortex neurons contributing to sensitivity to tones delivered in the presence of continuous noise. Hear Res 19: 253-268, 1985.
54. Pienkowski M, Eggermont J. Effects of adaptation on spectrotemporal receptive fields in primary auditory cortex. NeuroReport 20: 1198-1203, 2009.
55. Rust NC, Schwartz O, Movshon JA, Simoncelli EP. Spatiotemporal elements of macaque V1 receptive fields. Neuron 46: 945-956, 2005. (Pubitemid 40812353)
56. Sahani M, Linden JF. How linear are auditory cortical responses? In: Advances in Neural Information Processing Systems, edited by Becker S, Thrun S, Obermeyer K. Cambridge, MA: MIT Press, 2003, vol.15, p. 109-116.
57. Sanchez-Vives MV, Nowak LG, McCormick DA. Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J Neurosci 20: 4286-4299, 2000.
58. Scholl B, Gao X, Wehr M. Level dependence of contextual modulation in auditory cortex. J Neurophysiol 99: 1616-1627, 2008. (Pubitemid 351550060)
59. Schwartz O, Simoncelli EP. Natural signal statistics and sensory gain control. Nat Neurosci 4: 819-825, 2001. (Pubitemid 32702514)
60. Sharpee T, Rust NC, Bialek W. Analyzing neural responses to natural signals: maximally informative dimensions. Neural Comput 16: 223-250, 2004. (Pubitemid 38074494)
61. Simoncelli EP, Pillow J, Paninski L, Schwartz O. Characterization of neural responses with stochastic stimuli. In: The Cognitive Neurosciences III, edited by Gazzaniga M. Cambridge, MA: MIT Press, 2004, chapt. 23, p. 327-338.
62. 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. (Pubitemid 27130921)
63. 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. (Pubitemid 33626948)
64. Tsodyks MV, Markram H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94: 719-723, 1997. (Pubitemid 27053700)
65. Ulanovsky N, Las L, Farkas D, Nelken I. Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24: 10440-10453, 2004. (Pubitemid 39552629)
66. Ulanovsky N, Las L, Nelken I. Processing of low-probability sounds by cortical neurons. Nat Neurosci 6: 391-398, 2003. (Pubitemid 36373985)
67. van Lint JH. Introduction to Coding Theory. New York: Springer-Verlag, 1992.
68. Wehr M, Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446, 2003. (Pubitemid 37490130)
69. Wehr M, Zador AM. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47: 437-445, 2005. (Pubitemid 41073883)
70. Wu MCK, David SV, Gallant JL. Complete functional characterization of sensory neurons by system identification. Annu Rev Neurosci 29: 477-505, 2006.
71. Zador AM, Agmon-Snir H, Segev I. The morphoelectrotonic transform: a graphical approach to dendritic function. J Neurosci 15: 1669-1682, 1995.
72. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.