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

被引:28
作者
Avissar, Michael
Furman, Adam C.
Saunders, James C.
Parsons, Thomas D.
机构
[1] Univ Penn, Dept Clin Studies, Sch Vet Med, New Bolton Ctr, Kennett Sq, PA 19348 USA
[2] Univ Penn, Dept Otorhinolaryngol Head & Neck Surg, Sch Med, Kennett Sq, PA 19348 USA
关键词
auditory nerve; neural adaptation; hair cell; ribbon synapse; spike timing; neural variability;
D O I
10.1523/JNEUROSCI.5239-06.2007
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Sensory systems use adaptive coding mechanisms to filter redundant information from the environment to efficiently represent the external world. One such mechanism found in most sensory neurons is rate adaptation, defined as a reduction in firing rate in response to a constant stimulus. In auditory nerve, this form of adaptation is likely mediated by exhaustion of release-ready synaptic vesicles in the cochlear hair cell. To better understand how specific synaptic mechanisms limit neural coding strategies, we examined the trial-to-trial variability of auditory nerve responses during short-term rate-adaptation by measuring spike-timing precision and spike-count reliability. After adaptation, precision remained unchanged, whereas for all but the lowest-frequency fibers, reliability decreased. Modeling statistical properties of the hair cell-afferent fiber synapse suggested that the ability of one or a few vesicles to elicit an action potential reduces the inherent response variability expected from quantal neurotransmitter release, and thereby confers the observed count reliability at sound onset. However, with adaptation, depletion of the readily releasable pool of vesicles diminishes quantal content and antagonizes the postsynaptic enhancement of reliability. These findings imply that during the course of short-term adaptation, coding strategies that employ a rate code are constrained by increased neural noise because of vesicle depletion, whereas those that employ a temporal code are not.
引用
收藏
页码:6461 / 6472
页数:12
相关论文
共 70 条
[61]   SPONTANEOUS SYNAPTIC POTENTIALS FROM AFFERENT TERMINALS IN THE GUINEA-PIG COCHLEA [J].
SIEGEL, JH .
HEARING RESEARCH, 1992, 59 (01) :85-92
[62]   Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels [J].
Spassova, M ;
Eisen, MD ;
Saunders, JC ;
Parsons, TD .
JOURNAL OF PHYSIOLOGY-LONDON, 2001, 535 (03) :689-696
[63]   Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse [J].
Spassova, MA ;
Avissar, M ;
Furman, AC ;
Crumling, MA ;
Saunders, JC ;
Parsons, TD .
JARO-JOURNAL OF THE ASSOCIATION FOR RESEARCH IN OTOLARYNGOLOGY, 2004, 5 (04) :376-390
[64]   RATE FLUCTUATIONS AND FRACTIONAL POWER-LAW NOISE RECORDED FROM CELLS IN THE LOWER AUDITORY PATHWAY OF THE CAT [J].
TEICH, MC ;
JOHNSON, DH ;
KUMAR, AR ;
TURCOTT, RG .
HEARING RESEARCH, 1990, 46 (1-2) :41-52
[65]   PULSE-NUMBER DISTRIBUTION FOR THE NEURAL SPIKE TRAIN IN THE CATS AUDITORY-NERVE [J].
TEICH, MC ;
KHANNA, SM .
JOURNAL OF THE ACOUSTICAL SOCIETY OF AMERICA, 1985, 77 (03) :1110-1128
[66]   Precision of spike trains in primate retinal ganglion cells [J].
Uzzell, VJ ;
Chichilnisky, EJ .
JOURNAL OF NEUROPHYSIOLOGY, 2004, 92 (02) :780-789
[67]   Reproducibility and variability in neural spike trains [J].
vanSteveninck, RRD ;
Lewen, GD ;
Strong, SP ;
Koberle, R ;
Bialek, W .
SCIENCE, 1997, 275 (5307) :1805-1808
[68]   RAPID AND SHORT-TERM ADAPTATION IN AUDITORY-NERVE RESPONSES [J].
WESTERMAN, LA ;
SMITH, RL .
HEARING RESEARCH, 1984, 15 (03) :249-260
[69]   RATE RESPONSES OF AUDITORY-NERVE FIBERS TO TONES IN NOISE NEAR MASKED THRESHOLD [J].
YOUNG, ED ;
BARTA, PE .
JOURNAL OF THE ACOUSTICAL SOCIETY OF AMERICA, 1986, 79 (02) :426-442