The afferent synapse of cochlear hair cells
Introduction
The afferent synapse of mammalian cochlear hair cells is uniquely specialized in form and function. Individual afferent neurons in the peripheral (spiral) ganglion have a single unbranched dendrite that is postsynaptic to (usually) a solitary synaptic active zone of an inner hair cell (IHC). The active zone is demarcated by a slight thickening of the plasma membrane, and a collection of synaptic vesicles associated with the synaptic ribbon (Figure 1). The ribbon is a spherical or ellipsoidal electron-dense body, less than a micron in diameter, to which approximately 100 synaptic vesicles are tethered 1., 2.. This single synaptic structure carries the entire burden of acoustic signaling for each afferent neuron. Transmitter release from the hair cell triggers both sound-evoked, and spontaneous action potentials in afferent neurons (with spontaneous rates up to 140 per second) throughout the lifetime of the organism. In addition to this remarkable endurance, the hair cell’s afferent synapse also shows high temporal precision, releasing neurotransmitter to encode the submillisecond distinctions employed in sound localization (e.g. [3] reviewed in [4]). Somehow, similarly to retinal photoreceptors and bipolar cells, hair cells perform these feats of synaptic release without themselves generating action potentials. What parameters of ribbon structure and function confer these synaptic capabilities to hair cells? Here, we focus on insights arising from recent studies of hair cell synaptic function, but begin by reviewing ribbon structure and molecular composition.
Section snippets
Ribbon structure and molecular composition
The structure of synaptic ribbons in hair cells has been described by electron microscopy and more recently analyzed with 3-D tomography by Lenzi and co-workers 5., 6.••. In frog saccular hair cells the ribbon itself is an electron-dense sphere averaging 400 nm in diameter. Electron-lucent vesicles of about 35 nm diameter are either attached directly to the ribbon with 20 nm filaments or concentrated in the immediate surrounding cytoplasm by as yet unknown means. On the basis of capacitance
Ribbon function
Intracellular recording from hair cells has provided significant advances in this field, such as the capacitance measurements described below. Voltage-clamp recordings from the IHCs have also helped to identify two important molecular components of the synapse, the voltage-gated calcium channels that support transmitter release, and associated potassium channels that modulate excitability.
Conclusions
Several important steps have been taken in the study of the hair cell ribbon synapse over the past year. A firm description of the structural and functional basis of ribbon release will soon emerge from the combination of capacitance measurements with highly detailed ultrastructural studies, as exemplified by the analogy between slower components of release and outlier vesicles. Postsynaptic recordings from afferent boutons have nearly settled some questions, such as the functional
Update
The role of synaptic ribbons in transmitter release by hair cells has received additional confirmation in recent work by Zenisek and colleagues [47••]. These authors used calcium imaging methods and immunohistology to draw a compelling correspondence between sites of voltage-gated calcium influx and the synaptic ribbons of retinal bipolar cells and saccular hair cells. A fluorescent calcium indicator dye (Fluo-3 or Fluo 5F) was injected into hair cells along with a high concentration of calcium
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
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of special interest
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of outstanding interest
Acknowledgements
Work in the authors’ laboratories is supported by the National Institute of Deafness and Communication Disorders at the National Institutes of Health (P Fuchs and E Glowatzki), and by the Deutsche Forschungsgemeinschaft and the Max Planck Gesellschaft (T Moser).
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2018, Hearing ResearchCitation Excerpt :Like any other chemical synapse, a functional ribbon synapse consists of a presynaptic active zone and a postsynaptic density (review in Schnee and Ricci, 2017), which are closely aligned. However, the presynaptic element is an ellipsoid dense body, the ribbon (Fuchs et al., 2003; Nouvian et al., 2006), located at the base of the hair cell, which is anchored to the plasma membrane via lamellar sheets (Piatigorsky, 2001). In addition, every ribbon is surrounded by many vesicles that contain the excitatory neurotransmitter glutamate (Meyer et al., 2009).