title: Refractoriness enhances temporal coding by auditory nerve fibers.
abstract: A universal property of spiking neurons is refractoriness, a transient decrease in discharge probability immediately following an action potential (spike). The refractory period lasts only one to a few milliseconds, but has the potential to affect temporal coding of acoustic stimuli by auditory neurons, which are capable of submillisecond spike-time precision. Here this possibility was investigated systematically by recording spike times from chicken auditory nerve fibers in vivo while stimulating with repeated pure tones at characteristic frequency. Refractory periods were tightly distributed, with a mean of 1.58 ms. A statistical model was developed to recapitulate each fiber's responses and then used to predict the effect of removing the refractory period on a cell-by-cell basis for two largely independent facets of temporal coding: faithful entrainment of interspike intervals to the stimulus frequency and precise synchronization of spike times to the stimulus phase. The ratio of the refractory period to the stimulus period predicted the impact of refractoriness on entrainment and synchronization. For ratios less than ∼0.9, refractoriness enhanced entrainment and this enhancement was often accompanied by an increase in spike-time precision. At higher ratios, little or no change in entrainment or synchronization was observed. Given the tight distribution of refractory periods, the ability of refractoriness to improve temporal coding is restricted to neurons responding to low-frequency stimuli. Enhanced encoding of low frequencies likely affects sound localization and pitch perception in the auditory system, as well as perception in nonauditory sensory modalities, because all spiking neurons exhibit refractoriness.
authors: Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
authors: Michael
authors: M
authors: Avissar
authors: John H
authors: JH
authors: Wittig
authors: James C
authors: JC
authors: Saunders
authors: Thomas D
authors: TD
authors: Parsons
mesh_terms: D000161:Acoustic Stimulation; D000200:Action Potentials / Q000502:physiology; D000818:Animals; D000831:Animals, Newborn; D001306:Auditory Pathways / Q000502:physiology*; D002645:Chickens; D003056:Cochlear Nerve / Q000502:physiology*; D005260:Female; D008297:Male; D011930:Reaction Time / Q000502:physiology; D012032:Refractory Period, Electrophysiological / Q000502:physiology*; D011984:Sensory Receptor Cells / Q000502:physiology; D013997:Time Factors
references: IEEE Trans Neural Netw. 2004 Sep;15(5):1100-11
references: 15484887
references: Biophys J. 1967 Nov;7(6):759-77
references: 19210997
references: J Exp Biol. 1997;200(Pt 12):1809-19
references: 9319720
references: J Physiol. 2001 Sep 15;535(Pt 3):689-96
references: 11559767
references: J Neurophysiol. 1986 Aug;56(2):261-86
references: 3760921
references: J Assoc Res Otolaryngol. 2004 Dec;5(4):376-90
references: 15675002
references: J Neurophysiol. 2005 Oct;94(4):2526-34
references: 16160093
references: Proc Natl Acad Sci U S A. 1988 Nov;85(21):8311-5
references: 3186725
references: J Neurosci. 2001 Jul 1;21(13):4593-9
references: 11425887
references: J Acoust Soc Am. 1983 Aug;74(2):493-501
references: 6311884
references: J Neurophysiol. 1982 Sep;48(3):856-73
references: 6290620
references: J Comput Neurosci. 2003 Jan-Feb;14(1):71-90
references: 12435925
references: Vision Res. 1984;24(9):943-8
references: 6506482
references: Hear Res. 1980 Jul;3(1):45-63
references: 7400048
references: J Acoust Soc Am. 1985 Jul;78(1 Pt 1):90-4
references: 2991355
references: Neural Plast. 1999;6(4):147-72
references: 10714267
references: Neuroscience. 2008 Jun 12;154(1):65-76
references: 18424004
references: Neuron. 2000 Sep;27(3):635-46
references: 11055444
references: J Neurophysiol. 2009 Jun;101(6):3169-91
references: 19357334
references: Nature. 1983 Aug 11-17;304(5926):538-41
references: 6603579
references: Nat Neurosci. 2000 Aug;3(8):786-90
references: 10903571
references: J Neurosci. 1998 Mar 15;18(6):2200-11
references: 9482804
references: J Neurosci. 1997 Dec 1;17(23):9133-44
references: 9364060
references: Eur J Neurosci. 2006 Oct;24(7):2003-10
references: 17067297
references: J Neurophysiol. 2004 Aug;92(2):780-9
references: 15277596
references: Acta Otolaryngol. 1977 Nov-Dec;84(5-6):352-60
references: 303426
references: Hear Res. 1993 Sep;69(1-2):151-62
references: 8226336
references: J Neurophysiol. 1994 Mar;71(3):1022-36
references: 8201399
references: J Acoust Soc Am. 1983 Nov;74(5):1392-8
references: 6643851
references: J Neurosci. 2007 Jun 13;27(24):6461-72
references: 17567807
references: Hear Res. 1991 Oct;55(2):143-66
references: 1757283
references: J Assoc Res Otolaryngol. 2003 Sep;4(3):294-311
references: 14690049
references: J Neurosci. 2004 Dec 15;24(50):11356-67
references: 15601942
references: J Neurophysiol. 1968 Mar;31(2):301-34
references: 4972033
references: Hear Res. 2001 Sep;159(1-2):101-16
references: 11520638
references: J Neurosci. 2001 Jul 15;21(14):5066-78
references: 11438582
references: J Neurophysiol. 2005 Oct;94(4):2512-25
references: 16160092
references: J Assoc Res Otolaryngol. 2002 Dec;3(4):488-98
references: 12072915
references: J Neurophysiol. 1967 Jul;30(4):769-93
references: 4962851
references: J Neurosci. 1997 May 1;17(9):3312-21
references: 9096164
references: J Acoust Soc Am. 1989 Jun;85(6):2504-13
references: 2745875
references: J Ultrastruct Res. 1961 Dec;5:523-56
references: 13914158
references: Physiol Behav. 2005 Oct 15;86(3):297-305
references: 16202434
references: J Neurophysiol. 2008 Oct;100(4):1724-39
references: 18667546
references: J Neurophysiol. 1969 Jul;32(4):613-36
references: 5810617
references: Hear Res. 1986;24(1):1-15
references: 3759671
references: J Physiol. 1952 Aug;117(4):500-44
references: 12991237
references: J Neurophysiol. 1993 Dec;70(6):2562-83
references: 8120599
references: Nature. 1993 May 6;363(6424):74-6
references: 8479539
references: J Comp Physiol A. 1985 Sep;157(2):161-81
references: 3837088