Tuning and Timing in Mammalian Type I Hair Cells and Calyceal Synapses

Abstract

Afferent nerve fibers in the central zones of vestibular epithelia form calyceal endings around type I hair cells and have phasic response properties that emphasize fast head motions. We investigated how stages from hair-cell transduction to calyceal spiking contribute tuning and timing to central (striolar)-zone afferents of the rat saccular epithelium. In an excised preparation, we deflected individual hair bundles with rigid probes driven with steps and sinusoids (0.5–500 Hz) and recorded whole-cell responses from hair cells and calyces at room temperature and body temperature. In immature hair cells and calyces (postnatal days, P, 1–4), tuning sharpened at each stage. Transducer adaptation and membrane charging time produced bandpass filtering of the receptor potential with best frequencies of 10–30 Hz and phase leads below 10 Hz. For small stimuli, electrical resonances sharply tuned the hair cell membrane in the frequency range 5–40 Hz. The synaptic delay of quantal transmission added a phase lag above 10 Hz. The influence of spike thresholds at the calyceal spike initiation stage sharpened tuning and advanced response phase. Two additional mechanisms strongly advanced response phase above 10 Hz when present: maturing (P7-9) type I hair cells acquired low-voltage-activated channels that shortened the rise time of the receptor potential, and some calyces had non-quantal transmission with little synaptic delay. By reducing response time, the identified inner-ear mechanisms (transducer adaptation, low-voltage-activated channels, non-quantal transmission, and spike triggering) may compensate for transmission delays in vestibular reflex pathways and help stabilize posture and gaze during rapid head motions.

Distribution of Na,K-ATPase α Subunits in Rat Vestibular Sensory Epithelia

“…Secondly, we observed no to weak NKAα3 immunoreactivity in nascent calyces in preparations from younger animals, suggesting a developmental lag in NKAα3 expression in afferent calyces. Reduced expression of NKAα3 in immature calyces would be expected to result in greater K + accumulation and might contribute to observed nonquantal transmission in type I afferent transmission in maturing preparations (Songer and Eatock 2013). Thirdly, we did not observe NKAα3 immunoreactivity in the support cells in either crista or macular sections or cells of the nonsensory region of the vestibular epithelia at either age (data not shown) also consistent with the expected neuronal localization of NKA α3.…”

Evidence that protons act as neurotransmitters at vestibular hair cell–calyx afferent synapses

“…Results show the importance of both morphology and endogenous pH buffering in determining pH kinetics in the cleft. nqEPSCs recorded in utricular calyces of immature rats (16) are considerably faster than in the adult turtle lagenar calyces examined here. The relatively small volume of the calyx synaptic cleft in young rats clearly would increase the speed of proton buildup relative to the turtle lagena (Fig.…”

“…Synaptic transmission between type II cells and their terminals is chemically mediated and quantal (12,13). Synaptic transmission between type I cells and their calyces has a quantal glutamatergic component (13)(14)(15)(16)(17) augmented by a nonquantal excitatory postsynaptic current (nqEPSC) (14,16). It was hypothesized previously that the ball-and-socket morphology of the hair cell-calyx terminal might lead to the nqEPSC through stimulus-evoked modulation of the ½K + within the synaptic cleft (18)(19)(20).…”

Discharge regularity in the turtle posterior crista: comparisons between experiment and theory

“…While conclusions are similar to those reached previously (Goldberg et al 1982, 1984, Smith and Goldberg 1986, they are now based on direct observations of underlying mechanisms, rather than on inferences from the responses to externally applied galvanic currents. Eventually, results with sharp electrodes will have to be extended to whole cell recordings from afferent terminals, but this will require that the synaptic activity in the latter situation be increased to approach physiological levels (Chatlani 2011;Chatlani and Goldberg 2011;Highstein et al 2012;Songer and Eatock 2013). A: log (spike gain) vs. log (CV*), t ϭ 3.3, P Ͻ 0.01; B: log (synaptic voltage) vs. log(CV*), t ϭ 0.35, P Ͼ 0.5; C: log(spike gain re synaptic voltage) vs. log(CV*), t ϭ 4.6, P Ͻ 0.001; A1: spike phase vs. log(CV*), t ϭ 4.9, P ϽϽ 0.001; B1: phase synaptic voltage vs. log(CV*), t ϭ 2.4, P Ͻ 0.05; C1: spike phase re synaptic voltage vs. log(CV*), t ϭ 1.6, P Ͼ 0.2.…”

“…Discharge regularity in the turtle posterior crista: comparisons between experiment and theory. J Neurophysiol 110: 2830 -2848, 2013. First published September 4, 2013 doi:10.1152/jn.00195.2013.-Intra-axonal recordings were made from bouton fibers near their termination in the turtle posterior crista.…”