Transmission Between Type II Hair Cells and Bouton Afferents in the Turtle Posterior Crista

Abstract

Synaptic activity was recorded with sharp microelectrodes during rest and during 0.3-Hz sinusoidal stimulation from bouton afferents identified by their efferent-mediated inhibitory responses. A glutamate antagonist, 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) decreased quantal size (qsize) while lowering external Ca(2+) decreased quantal rate (qrate). Miniature excitatory postsynaptic potentials (mEPSPs) had effective durations (qdur) of 3.5-5 ms. Their timing was consistent with Poisson statistics. Mean qsizes ranged in different units from 0.25 to 0.73 mV and mean qrates from 200 to 1,500/s; there was an inverse relation across the afferent population between qrate and qsize. qsize distributions were consistent with the independent release of variable-sized quanta. Channel noise, measured during AMPA-induced depolarizations, was small compared with quantal noise. Excitatory responses were larger than inhibitory responses. Peak qrates, which could approach 3,000/s, led peak excitatory mechanical stimulation by 40 degrees . Quantal parameters varied with stimulation phase with qdur and qsize being maximal during inhibitory stimulation. Voltage modulation (vmod) was in phase with qrate and had a peak depolarization of 1.5-3 mV. On average, 80% of vmod was accounted for by quantal activity; the remaining 20% was a nonquantal component that persisted in the absence of quantal activity. The extracellular accumulation of glutamate and K(+) are potential sources of nonquantal transmission and may provide a basis for the inverse relation between qrate and qsize. Comparison of the phases of synaptic and spike activity suggests that both presynaptic and postsynaptic mechanisms contribute to variations across afferents in the timing of spikes during sinusoidal stimulation.

Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista

“…Recordings were made from the posterior ampullary nerve just as it bifurcates to innervate the two hemicristae. The recording site was ϳ250 m from the neuroepithelium, a distance estimated to be just over one-quarter of a length constant (Holt et al, 2006).…”

“…Electrical stimulation of efferent fibers was used to classify afferents (Holt et al, 2006). All efferent fibers destined for the posterior crista, but none of its afferents, travel in the so-called cross-bridge, a nerve bundle running between the anterior and posterior divisions of the VIIIth nerve (Fayyazuddin et al, 1991).…”

“…Many efferent effects are exerted on hair cells and only indirectly affect quantal activity in the afferent nerve fiber. As has been described (Neher and Sakaba 2003;Holt et al, 2006), we used shot-noise theory to characterize such activity. The key assumptions of the theory, which have been verified (Holt et al, 2006), are that the shapes of individual quantal events are stereotyped and their timing is governed by Poisson statistics.…”

“…As has been described (Neher and Sakaba 2003;Holt et al, 2006), we used shot-noise theory to characterize such activity. The key assumptions of the theory, which have been verified (Holt et al, 2006), are that the shapes of individual quantal events are stereotyped and their timing is governed by Poisson statistics. According to Rice's (1944) extension of Campbell's theorem, the mean ( 1 ), variance ( 2 ), and the third central moment or skew ( 3 ) are related to the quantal rate (qrate, ), quantal size (qsize, h), and the shape of individual quanta [f(t), t Ն0] by the following:…”

Resting Discharge Patterns of Macular Primary Afferents in Otoconia-Deficient Mice

“…The discharge of the eighth nerve sensory neurons in the absence of stimulation is thought to arise from a steady excitation due to background calciumdependent release of neurotransmitter from presynaptic hair cells (Adrian 1943;Annoni et al 1984;Flock and Russel 1976;Furukawa et al 1972;Furukawa and Ishii 1967;Harris and Flock 1967;Holt et al 2006Holt et al , 2007Hudspeth 1986;Ishii et al 1971;Katz 1969;Rossi et al 1977;Schessel et al 1991;Siegel 1992;Siegel and Dallos 1986; see recent review by Fuchs and Parsons 2006 regarding the details of synaptic release and physiology). The release of chemical neurotransmitter into the synapse by hair cells is thought to produce a steady background excitation of primary afferent dendrites and in turn lead to action potential discharge patterns.…”