Synaptic responses to mechanical stimulation in calyceal and bouton type vestibular afferents studied in an isolated preparation of semicircular canal ampullae of chicken.
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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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-P4), 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 of 5-40 Hz. The synaptic delay of quantal transmission added a phase lag at frequencies 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: (1) maturing (P7-P9) type I hair cells acquired low-voltage-activated channels that shortened the rise time of the receptor potential and (2) some calyces had nonquantal transmission with little synaptic delay. By reducing response time, the identified inner-ear mechanisms (transducer adaptation, low-voltage-activated channels, nonquantal transmission, and spike triggering) may compensate for transmission delays in vestibular reflex pathways and help stabilize posture and gaze during rapid head motions.Journal of Neuroscience 02/2013; 33(8):3706-24. · 6.91 Impact Factor
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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.Frontiers in Human Neuroscience 01/2013; 7:612. · 2.91 Impact Factor
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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.Journal of Neuroscience 07/2011; 31(27):10101-14. · 6.91 Impact Factor