Synaptic responses to mechanical stimulation in calyceal and bouton type vestibular afferents studied in an isolated preparation of semicircular canal ampullae of chicken

National Institute for Physiological Sciences, Okazaki, Japan.
Experimental Brain Research (Impact Factor: 2.04). 02/1990; 80(3):475-88. DOI: 10.1007/BF00227989
Source: PubMed


Relationships between the response patterns of semicircular canal afferents to mechanical stimulation and the morphologies of their peripheral endings were investigated in an isolated preparation of the anterior semicircular canal ampulla of chicken, using a combination of electrical recording with intracellular injections of Lucifer Yellow CH. The hair bundle mechanical stimulus was applied in a diffuse manner by a glass rod vibrating in the nearby bathing medium. Two types of spike discharge patterns and postsynaptic potentials were recorded. One type was found exclusively in the bouton type afferent and demonstrated a phasic increase of firing frequency and transient depolarizing postsynaptic potentials at the beginning of mechanical stimulation. These synaptic potentials were also observed spontaneously and their amplitudes were increased by membrane hyperpolarization. The other type was found exclusively in afferents with calyceal endings and showed a tonic increase of spiking frequency and depolarizing DC postsynaptic potentials with superimposing AC responses at the frequency of the mechanical stimulation. Amplitudes of postsynaptic potentials were increased by hyperpolarization. Hair cells generated depolarizing DC transduction potentials superimposed with AC potentials at frequency of the mechanical stimulation. The spontaneous spike discharging patterns of afferent nerve fibres were classified either as a regular type (CV less than 0.10) or as an irregular type (CV greater than 0.25) on the basis of coefficient of variation (CV) of interspike intervals. The spontaneous firing rate of regular units was higher than that of irregular units. Several membrane characteristics are different between these two types of afferent fibers; irregular units had short membrane time constants and fast spikes associated with clear spike-afterhyperpolarization. These features fit with the fact that irregular units tend to have phasic responses to mechanical stimulation while regular units typically have tonic responses. Irregular units had bouton endings with an average axonal diameter thicker than the regular units which had calix endings.

3 Reads
  • Source
    • "Interestingly, pannexin 1 channels have also been shown to function postsynaptically from pyramidal neurons (Thompson et al., 2008). Based on morphological arguments, an ephaptic mechanism has also been proposed for synaptic transmission between type I hair cells in the cochlea and the afferent calyx fiber (Hamilton, 1968; Gulley and Bagger-Sjoback, 1979; Yamashita and Ohmori, 1990; Goldberg, 1996). This synapse is also invaginating and thus creates the high resistance necessary for a functional ephapse. "
    [Show abstract] [Hide abstract]
    ABSTRACT: In the vertebrate retina, cones project to the horizontal cells (HCs) and bipolar cells (BCs). The communication between cones and HCs uses both chemical and ephaptic mechanisms. Cones release glutamate in a Ca(2+)-dependent manner, while HCs feed back to cones via an ephaptic mechanism. Hyperpolarization of HCs leads to an increased current through connexin hemichannels located on the tips of HC dendrites invaginating the cone synaptic terminals. Due to the high resistance of the extracellular synaptic space, this current makes the synaptic cleft slightly negative. The result is that the Ca(2+)-channels in the cone presynaptic membrane experience a slightly depolarized membrane potential and therefore more glutamate is released. This ephaptic mechanism forms a very fast and noise free negative feedback pathway. These characteristics are crucial, since the retina has to perform well in demanding conditions such as low light levels. In this mini-review we will discuss the critical components of such an ephaptic mechanism. Furthermore, we will address the question whether such communication appears in other systems as well and indicate some fundamental features to look for when attempting to identify an ephaptic mechanism.
    Full-text · Article · Sep 2013 · Frontiers in Human Neuroscience
  • Source
    • "A single calyx ending may receive input from tens of ribbons; in contrast, each bouton ending on a type II cell is generally driven by vesicular release from a single ribbon (Lysakowski and Goldberg, 1997, 2008; Holt et al., 2007). Type I calyx transmission also includes a nonquantal component of unknown mechanism (Yamashita and Ohmori, 1990; Holt et al., 2007), and retrograde vesicular transmission has been suggested (Scarfone et al., 1988; Devau et al., 1993; Scarfone et al., 1996; Chen and Eatock, 2000; Lysakowski and Singer, 2000). Cholinergic efferent terminals on calyx outer faces may provide positive feedback on afferent activity (Holt et al., 2011). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Many primary vestibular afferents form large cup-shaped postsynaptic terminals (calyces) that envelope the basolateral surfaces of type I hair cells. The calyceal terminals both respond to glutamate released from ribbon synapses in the type I cells and initiate spikes that propagate to the afferent's central terminals in the brainstem. The combination of synaptic and spike initiation functions in these unique sensory endings distinguishes them from the axonal nodes of central neurons and peripheral nerves, such as the sciatic nerve, which have provided most of our information about nodal specializations. We show that rat vestibular calyces express an unusual mix of voltage-gated Na and K channels and scaffolding, cell adhesion, and extracellular matrix proteins, which may hold the ion channels in place. Protein expression patterns form several microdomains within the calyx membrane: a synaptic domain facing the hair cell, the heminode abutting the first myelinated internode, and one or two intermediate domains. Differences in the expression and localization of proteins between afferent types and zones may contribute to known variations in afferent physiology.
    Full-text · Article · Jul 2011 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
  • Source
    • "Second, we described variations in quantal size and shape as quantal rate is varied by mechanical stimulation. Third, we investigated whether transmission between hair cells and their afferents includes nonquantal components, as had been previously suggested for transmission involving type I hair cells and calyx endings (Goldberg 1996; Yamashita and Ohmori 1990). Fourth, by comparing the phases of spike and quantal activity, we estimated the presynaptic (hair-cell) and postsynaptic (afferent ) contribution to variations in the timing of discharge across the afferent population. "
    [Show abstract] [Hide abstract]
    ABSTRACT: In the mammalian vestibular nerve, some afferents have highly irregular interspike intervals and others have highly regular intervals. To investigate whether spike timing is determined by the afferents' ion channels, we studied spiking activity in their cell bodies, isolated from the vestibular ganglia of young rats. Whole cell recordings were made with the perforated-patch method. As previously reported, depolarizing current steps revealed distinct firing patterns. Transient neurons fired one or two onset spikes, independent of current level. Sustained neurons were more heterogeneous, firing either trains of spikes or a spike followed by large voltage oscillations. We show that the firing pattern categories are robust, occurring at different temperatures and ages, both in mice and in rats. A difference in average resting potential did not cause the difference in firing patterns, but contributed to differences in afterhyperpolarizations. A low-voltage-activated potassium current (I(LV)) was previously implicated in the transient firing pattern. We show that I(LV) grew from the first to second postnatal week and by the second week comprised Kv1 and Kv7 (KCNQ) components. Blocking I(LV) converted step-evoked firing patterns from transient to sustained. Separated from their normal synaptic inputs, the neurons did not spike spontaneously. To test whether the firing-pattern categories might correspond to afferent populations of different regularity, we injected simulated excitatory postsynaptic currents at pseudorandom intervals. Sustained neurons responded to a given pattern of input with more regular firing than did transient neurons. Pharmacological block of I(LV) made firing more regular. Thus ion channel differences that produce transient and sustained firing patterns in response to depolarizing current steps can also produce irregular and regular spike timing.
    Full-text · Article · Oct 2010 · Journal of Neurophysiology
Show more