Time and intensity coding at the hair cell's ribbon synapse

Abstract

The activity of individual afferent neurones in the mammalian cochlea can be driven by neurotransmitter released from a single synaptic ribbon in a single inner hair cell. Thus, a ribbon synapse must be able to transmit all the information on sound frequency, intensity and timing carried centrally. This task is made still more demanding by the process of binaural sound localization that utilizes separate computations of time and intensity, with temporal resolution as fine as 10 micros in central nuclei. These computations may rely in part on the fact that the response phase (at the characteristic frequency) of individual afferent neurones is invariant with intensity. Somehow, the ribbon synapse can provide stronger synaptic drive to signal varying intensity, without accompanying changes in transmission time that ordinarily occur during chemical neurotransmission. Recent ultrastructural and functional studies suggest features of the ribbon that may underlie these capabilities.

Figure 1. Intensity invariant response phase

Histograms showing timing of action potentials in a single auditory afferent neurone during presentation of a tone at the characteristic frequency (1000 Hz). The time of peak firing remains constant as intensity changes from 10 to 90 dB. (From Rose et al. 1967; with permission.)

Figure 2. The ribbon synapse

A, transmission electron micrograph of a synaptic ribbon of an inner (cochlear) hair cell in a 2-month-old rat. The electron-dense ribbon is surrounded by a halo of small vesicles (∼30 nm diameter). The plasma membranes are thickened beneath the ribbon, that of the postsynaptic afferent neurone more obviously so. (Micrograph by T. Pongstaphone, unpublished.) B, ribbon schematic showing vesicles tethered to the dense body (ribbon), with one vesicle having fused to plasma membrane to release its contents (grey ‘cloud’ flattened by adjoining postsynaptic membrane).

Figure 3. EPSCs in cochlear afferents

A, excitatory postsynaptic currents recorded from afferent boutons at their point of contact with the inner hair cell. Membrane potential –94 mV. B, cumulative EPSC amplitude plots constructed from 3 different afferent fibres with different mean rates of release. Fibre no. 4 was measured in ‘normal’ conditions where membrane potentials are –60 mV on average. Fibre no. 2 was bathed in 40 mm K⁺ saline, which depolarized hair cells to ∼–35 mV. Fibre no. 8 had ‘bursting’ EPSCs whose timing suggested that they were produced by calcium action potentials in the neonatal hair cell. These exemplar recordings illustrate the fact that release probability did not correlate with EPSC amplitude distribution. (From Glowatzki & Fuchs, 2002; with permission; ©Nature Publishing Group, http:///www.nature.com).