A model of synaptic vesicle-pool depletion and replenishment can account for the interspike interval distributions and nonrenewal properties of spontaneous spike trains of auditory-nerve fibers

Journal of Neuroscience

Volumn 34, Issue 45, 2014, Pages 15097-15109

  Peterson, Adam J ^a   Irvine, Dexter R F ^b,c   Heil, Peter ^a,d  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b MONASH UNIVERSITY   (Australia)

^c BIONICS INSTITUTE   (Australia)

^d CENTER FOR BEHAVIORAL BRAIN SCIENCES   (Germany)

Author keywords

Auditory nerve; Fano factor; Interspike interval; Ribbon synapse; Serial correlation; Spontaneous activity

Indexed keywords

NEUROTRANSMITTER;

ACOUSTIC NERVE FIBER; ARTICLE; DATA ANALYSIS; MATHEMATICAL COMPUTING; NERVE CELL STIMULATION; REFRACTORY PERIOD; REGULATORY MECHANISM; SIMULATION; SPIKE WAVE; SYNAPSE; SYNAPSE VESICLE; ANIMAL; BIOLOGICAL MODEL; COCHLEAR NERVE; EXOCYTOSIS; METABOLISM; PHYSIOLOGY; SYNAPTIC POTENTIAL;

ANIMALS; COCHLEAR NERVE; EXOCYTOSIS; MODELS, NEUROLOGICAL; SYNAPTIC POTENTIALS; SYNAPTIC VESICLES;

EID: 84908543694     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0903-14.2014     Document Type: Article

References (71)

1. Amarasingham A, Chen TL, Geman S, Harrison MT, Sheinberg DL (2006) Spike count reliability and the Poisson hypothesis. J Neurosci 26:801-809. CrossRef Medline
2. Avila-Akerberg O, Chacron MJ (2011) Nonrenewal spike train statistics: causes and functional consequences on neural coding. Exp Brain Res 210:353-371. CrossRef Medline
3. Brown MC (1994) The antidromic compound action potential of the auditory nerve. J Neurophysiol 71:1826-1834.Medline
4. Carney LH (1993) A model for the responses of low-frequency auditorynerve fibers in cat. J Acoust Soc Am 93:401-417. CrossRef Medline
5. Cartee LA, van den Honert C, Finley CC, Miller RL (2000) Evaluation of a model of the cochlear neural membrane. I. Physiological measurement of membrane characteristics in response to intrameatal electrical stimulation. Hear Res 146:143-152. CrossRef Medline
6. Chacron MJ, Longtin A, St-Hilaire M, Maler L (2000) Suprathreshold stochastic firing dynamics with memory in P-type electroreceptors. Phys Rev Lett 85:1576-1579. CrossRef Medline
7. Chacron MJ, Longtin A, Maler L (2001) Negative interspike interval correlations increase the neuronal capacity for encoding time-dependent stimuli. J Neurosci 21:5328-5343. Medline
8. Cox DR (1962) Renewal theory. London: Methuen.
9. Cox DR, Lewis PAW (1966) The statistical analysis of series of events. London: Methuen.
10. Delgutte B (1996) Physiological models for basic auditory percepts. In: Auditory computation (Hawkins HL, McMullen TA, Popper AN, Fay RR, eds), pp 157-220. New York: Springer.
11. Doiron B, Chacron MJ, Maler L, Longtin A, Bastian J (2003) Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli. Nature 421:539-543. CrossRef Medline
12. Engel TA, Schimansky-Geier L, Herz AV, Schreiber S, Erchova I (2008) Subthreshold membrane-potential resonances shape spike-train patterns in the entorhinal cortex. J Neurophysiol 100:1576-1589. CrossRef Medline
13. Fano U (1947) Ionization yield of radiation. II. The fluctuations of the number of ions. Phys Rev 72:26-29. CrossRef
14. 2+signals and their heterogeneity in hair cells. Proc Natl Acad Sci U S A 106:4483-4488. CrossRef Medline
15. Gabbiani F, Koch C (1998) Principles of spike train analysis. In: Methods in neuronal modeling: from ions to networks (Koch C, Segev I, eds), pp 313-360. Cambridge, MA: MIT.
16. Gaumond RP, Kim DO, Molnar CE (1983) Responses of cochlear nerve fibers to brief acoustic stimuli: role of discharge history effects. J Acoust Soc Am 74:1392-1398. CrossRef Medline
17. Geisler CD, Goldberg JM (1966) A stochastic model of the repetitive activity of neurons. Biophys J 6:53-69. CrossRef Medline
18. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147-154. CrossRef Medline
19. Goldman MS, Maldonado P, Abbott LF (2002) Redundancy reduction and sustained firing with stochastic depressing synapses. J Neurosci 22:584-591.Medline
20. Grant L, Yi E, Glowatzki E (2010) Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. J Neurosci 30:4210-4220. CrossRef Medline
21. 2+nanodomains beneath the ribbon promote highly synchronous multivesicular release at hair cell synapses. J Neurosci 31:16637-16650. CrossRef Medline
22. Green DM, Swets JA (1966) Signal detection theory and psychophysics. New York: Wiley.
23. Heil P, Neubauer H (2001) Temporal integration of sound pressure determines thresholds of auditory-nerve fibers. J Neurosci 21:7404-7415.Medline
24. 2+-dependencies of exocytosis by receptor cells. Front Synaptic Neurosci 2:148. CrossRef Medline
25. Heil P, Neubauer H, Irvine DR, Brown M (2007) Spontaneous activity of auditory-nerve fibers: insights into stochastic processes at ribbon synapses. J Neurosci 27:8457-8474. CrossRef Medline
26. Heil P, Neubauer H, Brown M, Irvine DR (2008) Towards a unifying basis of auditory thresholds: distributions of the first-spike latencies of auditory-nerve fibers. Hear Res 238:25-38. CrossRef Medline
27. Heil P, Neubauer H, Irvine DR (2011) An improved model for the rate-level functions of auditory-nerve fibers. J Neurosci 31:15424-15437. CrossRef Medline
28. 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. CrossRef Medline
29. Johnson DH (1996) Point process models of single-neuron discharges. J Comput Neurosci 3:275-299. CrossRef Medline
30. Johnson DH, Tsuchitani C, Linebarger DA, Johnson MJ (1986) Application of a point process model to responses of cat lateral superior olive units to ipsilateral tones. Hear Res 21:135-159. CrossRef Medline
31. Kantardzhieva A, Liberman MC, Sewell WF (2013) Quantitative analysis of ribbons, vesicles, and cisterns at the cat inner hair cell synapse: correlations with spontaneous rate. J Comp Neurol 521:3260-3271. CrossRef Medline
32. Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889-894. CrossRef Medline
33. Kiang NYS, Watanabe T, Thomas EC, Clark LF (1965) Discharge patterns of single fibers in the cat’s auditory nerve. Research monographs 35. Cambridge, MA: MIT.
34. 2+channels and exocytosis at sensory synapses. J Physiol 591:3167-3178.Medline
35. Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119-132.Medline
36. Lenzi D, Crum J, Ellisman MH, Roberts WM (2002) Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 36:649-659. CrossRef Medline
37. Li J, Young ED (1993) Discharge-rate dependence of refractory behavior of cat auditory-nerve fibers. Hear Res 69:151-162. CrossRef Medline
38. Liberman MC (1978) Auditory-nerve responses from cats raised in a lownoise chamber. J Acoust Soc Am 63:442-455. CrossRef Medline
39. Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol 301:443-460. CrossRef Medline
40. Lowen SB, Teich MC (1991) Doubly stochastic point process driven by fractal shot noise. Phys Rev A 43:4192-4215. CrossRef Medline
41. Lowen SB, Teich MC (1992) Auditory-nerve action potentials form a nonrenewal point process over short as well as long time scales. J Acoust Soc Am 92:803-806. CrossRef Medline
42. Matthews G, Fuchs P (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11:812-822. CrossRef Medline
43. Miller CA, Abbas PJ, Robinson BK (2001) Response properties of the refractory auditory nerve fiber. J Assoc Res Otolaryngol 2:216-232.Medline
44. Miller MI, Wang J (1993) A new stochastic model for auditory-nerve discharge. J Acoust Soc Am 94:2093-2107. CrossRef Medline
45. Morsnowski A, Charasse B, Collet L, Killian M, Müller-Deile J (2006) Measuring the refractoriness of the electrically stimulated auditory nerve. Audiol Neurootol 11:389-402. CrossRef Medline
46. Moser T, Neef A, Khimich D (2006) Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J Physiol 576:55-62. CrossRef Medline
47. Neubauer H, Köppl C, Heil P (2009) Spontaneous activity of auditory nerve fibers in the barn owl (Tyto alba): analyses of interspike interval distributions. J Neurophysiol 101:3169-3191. CrossRef Medline
48. Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbons synapse. J Membr Biol 209:153-165. CrossRef Medline
49. Rajdl K, Lansky P (2014) Fano factor estimation. Math Biosci Eng 11:105-123. CrossRef Medline
50. Ratnam R, Nelson ME (2000) Nonrenewal statistics of electrosensory afferent spike trains: implications for the detection of weak sensory signals. J Neurosci 20:6672-6683.Medline
51. Rutherford MA, Chapochnikov NM, Moser T (2012) Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. J Neurosci 32:4773-4789. CrossRef Medline
52. Schwalger T, Lindner B (2010) Theory for serial correlations of interevent intervals. Eur Phys J Special Topics 187:211-221. CrossRef
53. Shepherd RK, Roberts LA, Paolini AG (2004) Long-term sensorineural hearing loss induces functional changes in rat auditory nerve. Eur J Neurosci 20:3131-3140. CrossRef Medline
54. Siegel JH (1992) Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea. Hear Res 59:85-92. CrossRef Medline
55. Sumner CJ, Lopez-Poveda EA, O’Mard LP, Meddis R (2002) A revised model of the inner-hair cell and auditory-nerve complex. J Acoust Soc Am 111:2178-2188. CrossRef Medline
56. Sumner CJ, Lopez-Poveda EA, O’Mard LP, Meddis R (2003) Adaptation in a revised inner-hair cell model. J Acoust Soc Am 113:893-901. CrossRef Medline
57. Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93:557-569.Medline
58. Teich MC (1989) Fractal character of the auditory neural spike train. IEEE Trans Biomed Eng 36:150-160. CrossRef Medline
59. 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. CrossRef Medline
60. Teich MC, Turcott RG, Lowen SB (1990) The fractal doubly stochastic Poisson point process as a model for the cochlear neural spike train. In: The mechanics and biophysics of hearing (Dallos P, Geisler CD, Matthews JW, Ruggero MA, Steele CR, eds), pp 354-361. New York: Springer.
61. Tsuchitani C, Johnson DH (1985) The effects of ipsilateral tone-burst stimulus level on the discharge patterns of cat lateral superior olivary units. J Acoust Soc Am 77:1484-1496. CrossRef Medline
62. Urdapilleta E (2011) Onset of negative interspike interval correlations in adapting neurons. Phys Rev E Stat Nonlin Soft Matter Phys 84:041904. CrossRef Medline
63. Wang XJ (1998) Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J Neurophysiol 79:1549-1566.Medline
64. Winter IM, Robertson D, Yates GK (1990) Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres. Hear Res 45:191-202. CrossRef Medline
65. 2+influx to exocytosis. EMBO J 33:247-264. CrossRef Medline
66. Wu J, Young ED, Glowatzki E (2014) Simultaneous recordings of pairs of auditory nerve fibers contacting the same inner hair cell. Abstr Assoc Res Otolaryngol PS-224.
67. Yates GK (1991) Auditory-nerve spontaneous rates vary predictably with threshold. Hear Res 57:57-62. CrossRef Medline
68. 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. CrossRef Medline
69. 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. CrossRef Medline
70. Zilany MS, 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. CrossRef Medline
71. Zilany MS, 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. CrossRef Medline