Adaptation reduces spike-count reliability, but not spike-timing precision, of auditory nerve responses

Journal of Neuroscience

Volumn 27, Issue 24, 2007, Pages 6461-6472

  Avissar, Michael ^a   Furman, Adam C ^a   Saunders, James C ^a   Parsons, Thomas D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Auditory nerve; Hair cell; Neural adaptation; Neural variability; Ribbon synapse; Spike timing

Indexed keywords

NEUROTRANSMITTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; COCHLEAR NERVE; CONTROLLED STUDY; HAIR CELL; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SENSORY SYSTEM; SYNAPSE VESICLE;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; AUDITORY THRESHOLD; CHICK EMBRYO; CHICKENS; COCHLEAR NERVE; DOSE-RESPONSE RELATIONSHIP, RADIATION; MONTE CARLO METHOD; NEURONS, AFFERENT; POISSON DISTRIBUTION; REACTION TIME; TIME FACTORS;

EID: 34250327500     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5239-06.2007     Document Type: Article

References (70)

1. Adrian ED, Zotterman Y (1926) The impulses produced by sensory nerve endings: II. The response of a single end organ. J Physiol (Lond) 61:151-171.
2. Anderson DJ, Rose JE, Hind JE, Brugge JF (1971) Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: frequency and intensity effects. J Acoust Soc Am 49:1131-1139.
3. Barlow HB (1961) Possible principles underlying the transformations of sensory messages. In: Sensory communication (Rosenblith WA, ed), pp 217-234. Cambridge, MA: MIT.
4. Berry MJ, Warland DK, Meister M (1997) The structure and precision of retinal spike trains. Proc Natl Acad Sci USA 94:5411-5416.
5. Berry II MJ, Meister M (1998) Refractoriness and neural precision. J Neurosci 18:2200-2211.
6. Beutner D, Moser T (2001) The presynaptic function of mouse cochlear inner hair cells during development of hearing. J Neurosci 21:4593-4599.
7. Brenner N, Bialek W, de Ruyter van Steveninck R (2000) Adaptive rescaling maximizes information transmission. Neuron 26:695-702.
8. Buracas GT, Zador AM, DeWeese MR, Albright TD (1998) Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20:959-969.
9. Colburn HS, Carney LH, Heinz MG (2003) Quantifying the information in auditory-nerve responses for level discrimination. J Assoc Res Otolaryngol 4:294-311.
10. Collias N, Joos M (1953) The spectrographic analysis of sound signals of the domestic fowl. Behaviour 5:175-187.
11. 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.
12. Crumling MA, Saunders JC (2007) Tonotopic distribution of short-term adaptation properties in the cochlear nerve of normal and acoustically overexposed chicks. J Assoc Res Otolaryngol 8:54-68.
13. Cummings DD, Wilcox KS, Dichter MA (1996) Calcium-dependent paired-pulse facilitation of miniature EPSC frequency accompanies depression of EPSCs at hippocampal synapses in culture. J Neurosci 16:5312-5323.
14. 2+ uptake prevents desynchronization of quantal release and minimizes depletion during repetitive stimulation of mouse motor nerve terminals. J Physiol (Lond) 548:425-438.
15. de Ruyter van Steveninck RR, Lewen GD, Strong SP, Koberle R, Bialek W (1997) Reproducibility and variability in neural spike trains. Science 275:1805-1808.
16. Dean I, Harper NS, McAlpine D (2005) Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8:1684-1689.
17. Del Castillo J, Katz B (1954) Quantal components of the end-plate potential. J Physiol (Lond) 124:560-573.
18. Delgutte B (1980) Representation of speech-like sounds in the discharge patterns of auditory-nerve fibers. J Acoust Soc Am 68:843-857.
19. DeWeese MR, Wehr M, Zador AM (2003) Binary spiking in auditory cortex. J Neurosci 23:7940-7949.
20. 2+-ATPase isoform 2a is the PMCA of hair bundles. J Neurosci 21:5066-5078.
21. Edmonds B, Reyes R, Schwaller B, Roberts WM (2000) Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786-790.
22. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792.
23. Fano U (1947) Ionization yield of radiations. II. The fluctuations of the number of ions. Physiol Rev 72:26-29.
24. Fukui I, Sato T, Ohmori H (2006) Improvement of phase information at low sound frequency in nucleus magnocellularis of the chicken. J Neurophysiol 96:633-641.
25. Furman AC, Avissar M, Saunders JC (2006) The effects of intense sound exposure on phase locking in the chick (Gallus domesticus) cochlear nerve. Eur J Neurosci 24:2003-2010.
26. 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 (Lond) 276:211-226.
27. Gaumond RP, Kim DO, Molnar CE (1983) Response of cochlear nerve fibers to brief acoustic stimuli: role of discharge-history effects. J Acoust Soc Am 74:1392-1398.
28. Geisler CD (1981) A model for discharge patterns of primary auditory-nerve fibers. Brain Res 212:198-201.
29. Gibson DJ, Young ED, Costalupes JA (1985) Similarity of dynamic range adjustment in auditory nerve and cochlear nuclei. J Neurophysiol 53:940-958.
30. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147-154.
31. Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613-636.
32. Gray PR (1967) Conditional probability analyses of the spike activity of single neurons. Biophys J 7:759-777.
33. Hagler Jr DJ, Goda Y (2001) Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. J Neurophysiol 85:2324-2334.
34. Heinz MG, Colburn HS, Carney LH (2001) Evaluating auditory performance limits: I. One-parameter discrimination using a computational model for the auditory nerve. Neural Comput 13:2273-2316.
35. 2+ buffer in hair cells. J Assoc Res Otolaryngol 3:488-498.
36. Hill KG, Stange G, Mo J (1989) Temporal synchronization in the primary auditory response in the pigeon. Hear Res 39:63-73.
37. Hillery CM, Narins PM (1987) Frequency and time domain comparison of low-frequency auditory fiber responses in two anuran amphibians. Hear Res 25:233-248.
38. Jensen K, Jensen MS, Lambert JD (1999) Post-tetanic potentiation of GABAergic IPSCs in cultured rat hippocampal neurones. J Physiol (Lond) 519:71-84.
39. Jensen K, Lambert JD, Jensen MS (2000) Tetanus-induced asynchronous GABA release in cultured hippocampal neurons. Brain Res 880:198-201.
40. Johnson DH (1980) The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J Acoust Soc Am 68:1115-1122.
41. Johnson DH, Kiang NY (1976) Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers. Biophys J 16:719-734.
42. Johnson DH, Swami A (1983) The transmission of signals by auditory-nerve fiber discharge patterns. J Acoust Soc Am 74:493-501.
43. Kass RE, Ventura V, Brown EN (2005) Statistical issues in the analysis of neuronal data. J Neurophysiol 94:8-25.
44. Kelly OE, Johnson DH, Delgutte B, Cariani P (1996) Fractal noise strength in auditory-nerve fiber recordings. J Acoust Soc Am 99:2210-2220.
45. Kiang NY (1965) Discharge patterns of single fibers in the cat's auditory nerve. Cambridge, MA: MIT.
46. 2+ concentration and asynchronous transmitter release at single GABAergic boutons in rat collicular cultures. J Physiol (Lond) 548:753-764.
47. Köppl C (1997) Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17:3312-3321.
48. Laughlin SB (1989) The role of sensory adaptation in the retina. J Exp Biol 146:39-62.
49. Lewis RS, Hudspeth AJ (1983) Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature 304:538-541.
50. Lowen SB, Teich MC (1992) Auditory-nerve action potentials form a non-renewal point process over short as well as long time scales. J Acoust Soc Am 92:803-806.
51. Lu T, Trussell LO (2000) Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26:683-694.
52. 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 USA 97:883-888.
53. Palmer AR, Russell IJ (1986) Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells. Hear Res 24:1-15.
54. Paolini AG, FitzGerald JV, Burkitt AN, Clark GM (2001) Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat. Hear Res 159:101-116.
55. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. I. The single spike train. Biophys J 7:391-418.
56. Rieke F, Warland DK, de Ruyter van Steveninck RR, Bialek W (1997) Spikes: exploring the neural code. Cambridge, MA: MIT.
57. Roberts WM (1993) Spatial calcium buffering in saccular hair cells. Nature 363:74-76.
58. Rokem A, Watzl S, Gollisch T, Stemmler M, Herz AV, Samengo I (2006) Spike-timing precision underlies the coding efficiency of auditory receptor neurons. J Neurophysiol 95:2541-2552.
59. Rose JE, Brugge JF, Anderson DJ, Hind JE (1967) Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J Neurophysiol 30:769-793.
60. Saunders JC, Doan DE, Poje CP, Fisher KA (1996) Cochlear nerve activity after intense sound exposure in neonatal chicks. J Neurophysiol 76:770-787.
61. Schaette R, Gollisch T, Herz AV (2005) Spike-train variability of auditory neurons in vivo: dynamic responses follow predictions from constant stimuli. J Neurophysiol 93:3270-3281.
62. Siegel JH (1992) Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea. Hear Res 59:85-92.
63. Spassova M, Eisen MD, Saunders JC, Parsons TD (2001) Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. J Physiol (Lond) 535:689-696.
64. 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.
65. Teich MC, Khanna SM (1985) Pulse-number distribution for the neural spike train in the cat's auditory nerve. J Acoust Soc Am 77:1110-1128.
66. Teich MC, Johnson DH, Kumar AR, Turcott RG (1990) Rate fluctuations and fractional power-law noise recorded from cells in the lower auditory pathway of the cat. Hear Res 46:41-52.
67. Uzzell VJ, Chichilnisky EJ (2004) Precision of spike trains in primate retinal ganglion cells. J Neurophysiol 92:780-789.
68. Westerman LA, Smith RL (1984) Rapid and short-term adaptation in auditory nerve responses. Hear Res 15:249-260.
69. Young ED, Barta PE (1986) Rate responses of auditory nerve fibers to tones in noise near masked threshold. J Acoust Soc Am 79:426-442.
70. Zador A (1998) Impact of synaptic unreliability on the information transmitted by spiking neurons. J Neurophysiol 79:1219-1229.