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      Transmitter release at the hair cell ribbon synapse.

      Nature neuroscience

      Action Potentials, physiology, Animals, Calcium, Excitatory Postsynaptic Potentials, Hair Cells, Auditory, metabolism, Hair Cells, Auditory, Inner, In Vitro Techniques, Nerve Fibers, Neurotransmitter Agents, Rats, Receptors, AMPA, Rest, Synapses

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          Abstract

          Neurotransmitters are released continuously at ribbon synapses in the retina and cochlea. Notably, a single ribbon synapse of inner hair cells provides the entire input to each cochlear afferent fiber. We investigated hair cell transmitter release in the postnatal rat cochlea by recording excitatory postsynaptic currents (EPSCs) from afferent boutons directly abutting the ribbon synapse. EPSCs were carried by rapidly gating AMPA receptors. EPSCs were clustered in time, indicating the possibility of coordinate release. Amplitude distributions of spontaneous EPSCs were highly skewed, peaking at 0.4 nS and ranging up to 20 times larger. Hair cell depolarization increased EPSC frequency up to 150 Hz without altering the amplitude distribution. We propose that the ribbon synapse operates by multivesicular release, possibly to achieve high-frequency transmission.

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          Most cited references 38

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          Expression of a potassium current in inner hair cells during development of hearing in mice.

          Excitable cells use ion channels to tailor their biophysical properties to the functional demands made upon them. During development, these demands may alter considerably, often associated with a change in the cells' complement of ion channels. Here we present evidence for such a change in inner hair cells, the primary sensory receptors in the mammalian cochlea. In mice, responses to sound can first be recorded from the auditory nerve and observed behaviourally from 10-12 days after birth; these responses mature rapidly over the next 4 days. Before this time, mouse inner hair cells have slow voltage responses and fire spontaneous and evoked action potentials. During development of auditory responsiveness a large, fast potassium conductance is expressed, greatly speeding up the membrane time constant and preventing action potentials. This change in potassium channel expression turns the inner hair cell from a regenerative, spiking pacemaker into a high-frequency signal transducer.
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            Single-neuron labeling in the cat auditory nerve.

             M. Liberman (1982)
            Single auditory nerve fibers in the cat were labeled intracellularly with horseradish peroxidase. The sample of fibers was selected to represent different response types over a wide range of characteristic frequencies. All 56 labeled neurons were found to be radial fibers innervating inner hair cells, suggesting that none of the single-unit data reported to date has been from the outer hair cell innervation. Differences in rates of spontaneous discharge and thresholds to tones among these labeled neurons were closely correlated with morphological differences in the caliber and location of their unmyelinated terminals on the body of the inner hair cell.
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              Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients.

              The cellular mechanisms responsible for large miniature currents in some brain synapses remain undefined. In Purkinje cells, we found that large-amplitude miniature inhibitory postsynaptic currents (mIPSCs) were inhibited by ryanodine or by long-term removal of extracellular Ca2+. Two-photon Ca2+ imaging revealed random, ryanodine-sensitive intracellular Ca2+ transients, spatially constrained at putative presynaptic terminals. At high concentration, ryanodine decreased action-potential-evoked rises in intracellular Ca2+. Immuno-localization showed ryanodine receptors in these terminals. Our data suggest that large mIPSCs are multivesicular events regulated by Ca2+ release from ryanodine-sensitive presynaptic Ca2+ stores.
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                Author and article information

                Journal
                11802170
                10.1038/nn796

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