Power-law dynamics in an auditory-nerve model can account for neural adaptation to sound-level statistics

Journal of Neuroscience

Volumn 30, Issue 31, 2010, Pages 10380-10390

  Zilany, Muhammad S A ^a,b   Carney, Laurel H ^a,b  

^a University of Rochester   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ARTICLE; COCHLEAR NERVE; COMPARATIVE STUDY; HAIR CELL; HYPOTHESIS; NERVE CELL; PRIORITY JOURNAL; RECEPTOR POTENTIAL; SOUND INTENSITY; SPIKE; SYNAPSE;

AUDITORY PATHWAYS; AUDITORY PERCEPTION; AUDITORY THRESHOLD; COCHLEAR NERVE; COMPUTER SIMULATION; MODELS, NEUROLOGICAL; SOUND;

EID: 77955388334     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0647-10.2010     Document Type: Article

References (51)

1. Backus BC, Guinan JJ Jr (2006) Time course of the human medial olivocochlear reflex. J Acoust Soc Am 119:2889-2904.
2. Bruce IC, Sachs MB, Young ED (2003) An auditory-periphery model of the effects of acoustic trauma on auditory nerve responses. J Acoust Soc Am 113:369-388.
3. Carney LH (1993) A model for the responses of low-frequency auditorynerve fibers in cat. J Acoust Soc Am 93:401-417.
4. Chapman KM, Smith RS (1963) A linear transfer function underlying impulse frequency modulation in a cockroach mechanoreceptor. Nature 197:699-700.
5. Colburn HS, Carney LH, Heinz MG (2003) Quantifying the information in auditory-nerve responses for level discrimination. J Assoc Res Otolaryngol 4:294-311.
6. Cooper NP, Yates GK (1994) Nonlinear input-output functions derived from the responses of guinea-pig cochlear nerve fibres: variations with characteristic frequency. Hear Res 78:221-234.
7. Costalupes JA, Young ED, Gibson DJ (1984) Effects of continuous noise backgrounds on rate response of auditory-nerve fibers in cat. J Neurophysiol 51:1326-1344.
8. Dean I, Harper NS, McAlpine D (2005) Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8:1684-1689.
9. Dean I, Robinson BL, Harper NS, McAlpine D (2008) Rapid neural adaptation to sound level statistics. J Neurosci 28:6430-6438.
10. Delgutte B (1990) Two-tone rate suppression in auditory-nerve fibers: dependence on suppressor frequency and level. Hear Res 49:225-246.
11. Drew PJ, Abbott LF (2006) Models and properties of power-law adaptation in neural system. J Neurophysiol 96:826-833.
12. French AS (1984) The receptor potential and adaptation in the cockroach tactile spine. J Neurosci 4:2063-2068.
13. French AS, Torkkeli PH (2008) The power law of sensory adaptation: simulation by a model of excitability in spider mechanoreceptor neurons. Ann Biomed Eng 36:153-161.
14. Furukawa T, Hayashida Y, Matsuura S (1978) Quantal analysis of the size of excitatory post-synaptic potentials at synapses between hair cells and afferent nerve fibres in goldfish. J Physiol 276:211-226. (Pubitemid 8298523)
15. Gibson DJ, Young ED, Costalupes JA (1985) Similarity of dynamic-range adjustment in auditory-nerve and cochlear nuclei. J Neurophysiol 53:940-958.
16. Goutman JD, Glowatzki E (2007) Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc Natl Acad Sci U S A 104:16341-16346.
17. Guinan JJ Jr (2006) Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear 27:589-607.
18. Harris DM, Dallos P (1979) Forward masking of auditory nerve fiber responses. J Neurophysiol 42:1083-1107.
19. Jackson BS, Carney LH (2005) The spontaneous-rate histogram of the auditory nerve can be explained by only two or three spontaneous rates and long-range dependence. J Assoc Res Otolaryngol 6:148-159.
20. Javel E (1981) Suppression of auditory-nerve responses. 1. Temporal analysis, intensity effects and suppression contours. J Acoust Soc Am 69:1735-1745.
21. Kiang NYS (1965) Discharge patterns of single fibers in the cat's auditory nerve. MIT Research Monograph No. 35. Boston: Technology Press.
22. Kiang NYS (1990) Curious oddments of auditory-nerve studies. Hear Res 49:1-16.
23. Kros CJ, Crawford AC (1990) Potassium currents in inner hair cells isolated from the guinea-pig cochlea. J Physiol 421:263-291.
24. La Camera G, Rauch A, Thurbon D, Lüscher HR, Senn W, Fusi S (2006) Multiple time scales of temporal response in pyramidal and fast spiking cortical neurons. J Neurophysiol 96:3448-3464.
25. Moser T, Beutner D (2000) Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci U S A 97:883-888.
26. Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbon synapse. J Membr Biol 209:153-165.
27. Patuzzi R (1996) Cochlear micromechanics and macromechanics. In: The cochlea (Dallos P, Popper AN, Fay RR, eds), pp 186-257. New York: Springer.
28. Pouille F, Marin-Burgin A, Adesnik H, Atallah BV, Scanziani M (2009) Input normalization by global feedforward inhibition expands cortical dynamic range. Nat Neurosci 12:1577-1585.
29. Raman IM, Zhang S, Trussell LO (1994) Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. J Neurosci 14:4998-5010.
30. Relkin EM, Doucet JR (1991) Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons. Hear Res 55:215-222.
31. Sachs MB, Abbas PJ (1974) Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J Acoust Soc Am 56:1835-1847.
32. Smith RL (1977) Short-term adaptation in single auditory-nerve fibers: some post-stimulatory effects. J Neurophysiol 40:1098-1111.
33. Smith RL, Zwislocki JJ (1975) Short-term adaptation and incremental responses of single auditory-nerve fibers. Biol Cybern 17:169-182.
34. Smith RL, Brachman ML, Frisina RD (1985) Sensitivity of auditory-nerve fibers to changes in intensity: a dichotomy between decrements and increments. J Acoust Soc Am 78:1310-1316.
35. Spassova MA, Avissar M, Furman AC, Crumling MA, Saunders JC, Parsons TD (2004) Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. J Assoc Res Otolaryngol 5:376-390.
36. Thorson J, Biederman-Thorson M (1974) Distributed relaxation processes in sensory adaptation. Science 183:161-172.
37. Viemeister NF (1983) Auditory intensity discrimination at high frequencies in the presence of noise. Science 221:1206-1208.
38. Viemeister NF (1988) Intensity coding and the dynamic range problem. Hear Res 34:267-274.
39. Watkins PV, Barbour DL (2008) Specialized neuronal adaptation for preserving input sensitivity. Nat Neurosci 11:1259-1261.
40. Wen B, Wang GI, Dean I, Delgutte B (2009) Dynamic range adaptation to sound level statistics in the auditory nerve. J Neurosci 29:13797-13808.
41. Westerman LA, Smith RL (1984) Rapid and short-term adaptation in auditory nerve responses. Hear Res 15:249-260.
42. Westerman LA, Smith RL (1988) A diffusion model of the transient response of the cochlear inner hair cell synapse. J Acoust Soc Am 83:2266-2276.
43. Winslow RL, Sachs MB (1988) Single-tone intensity discrimination based on auditory-nerve rate responses in backgrounds of quiet noise, and with stimulation of the crossed olivocochlear bundle. Hear Res 35:165-189.
44. Yates GK, Robertson D, Johnstone BM (1985) Very rapid adaptation in the guinea pig auditory nerve. Hear Res 17:1-12.
45. Young E, Sachs MB (1973) Recovery from sound exposure in auditorynerve fibers. J Acoust Soc Am 54:1535-1543.
46. Zhang F, Miller CA, Robinson BK, Abbas PJ, Hu N (2007) Changes across time in spike rate and spike amplitude of auditory nerve fibers simulated by electric pulse trains. J Assoc Res Otolaryngol 8:356-372.
47. Zhang X, Carney LH (2005) Analysis of models for the synapse between the inner hair cell and the auditory nerve. J Acoust Soc Am 118: 1540-1553.
48. Zhang X, Heinz MG, Bruce IC, Carney LH (2001) A phenomenological model for the responses of auditory-nerve fibers. I. Nonlinear tuning with compression and suppression. J Acoust Soc Am 109:648-670.
49. Zilany MSA, Bruce IC (2006) Modeling auditory-nerve responses for high sound pressure levels in the normal and impaired auditory periphery. J Acoust Soc Am 120:1446-1466.
50. Zilany MSA, Bruce IC (2007) Representation of the vowel /ε/ in normal and impaired auditory nerve fibers: model predictions of responses in cats. J Acoust Soc Am 122:402-417.
51. Zilany MSA, Bruce IC, Nelson PC, Carney LH (2009) A phenomenological model of the synapse between the inner hair cell and auditory nerve: long-term adaptation with power-law dynamics. J Acoust Soc Am 126: 2390-2412.