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: 2.17). 02/1990; 80(3):475-88. DOI: 10.1007/BF00227989
Source: PubMed

ABSTRACT 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.

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    • "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). "
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    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.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 07/2011; 31(27):10101-14. DOI:10.1523/JNEUROSCI.0521-11.2011 · 6.75 Impact Factor
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    • "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. "
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    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.
    Journal of Neurophysiology 10/2010; 104(4):2034-51. DOI:10.1152/jn.00396.2010 · 3.04 Impact Factor
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    • "The postsynaptic potential in a calyx receiving input of around 10 synaptic ribbons (type I hair cell) is only about three times larger than the postsynaptic potential of a single bouton receiving input from one synaptic ribbon (type II hair cell), suggesting that calyceal synapses are rather inefficient (Eatock et al., 1998). In addition, experiments using pharmacological inhibitors of glutamate receptors show calyx depolarization in the absence of formal synaptic transmission (Holt et al., 2007a; Yamashita and Ohmori, 1990). Goldberg has proposed a theoretical model correlating the narrow gap and the extent of the contact between the calyx and the type I hair cells to the unexplained properties of calyceal synapses, where the K + ions in the intercellular space affect calyceal transmission (Goldberg, 1996). "
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    ABSTRACT: The afferent innervation contacting the type I hair cells of the vestibular sensory epithelia form distinct calyceal synapses. The apposed presynaptic and postsynaptic membranes at this large area of synaptic contact are kept at a remarkably regular distance. Here, we show by freeze-fracture electron microscopy that a patterned alignment of proteins at the calyceal membrane resembles a type of intercellular junction that is rare in vertebrates, the septate junction (SJ). We found that a core molecular component of SJs, Caspr, colocalizes with the K(+) channel KCNQ4 at the postsynaptic membranes of these calyceal synapses. Immunolabeling and ultrastructural analyses of Caspr knock-out mice reveal that, in the absence of Caspr, the separation between the membranes of the hair cells and the afferent neurons is conspicuously irregular and often increased by an order of magnitude. In these mutants, KCNQ4 fails to cluster at the postsynaptic membrane and appears diffused along the entire calyceal membrane. Our results indicate that a septate-like junction provides structural support to calyceal synaptic contact with the vestibular hair cell and that Caspr is required for the recruitment or retention of KCNQ4 at these synapses.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 04/2009; 29(10):3103-8. DOI:10.1523/JNEUROSCI.4868-08.2009 · 6.75 Impact Factor
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