Cochlear hair cells: The sound-sensing machines

Abstract

The sensory epithelium of the mammalian inner ear contains two types of mechanosensory cells: inner (IHC) and outer hair cells (OHC). They both transduce mechanical force generated by sound waves into electrical signals. In their apical end, these cells possess a set of stereocilia representing the mechanosensing organelles. IHC are responsible for detecting sounds and transmitting the acoustic information to the brain by converting graded depolarization into trains of action potentials in auditory nerve fibers. OHC are responsible for the active mechanical amplification process that leads to the fine tuning and high sensitivity of the mammalian inner ear. This active amplification is the consequence of the ability of OHC to alter their cell length in response to changes in membrane potential, and is controlled by an efferent inhibitory innervation. Medial olivocochlear efferent fibers, originating in the brainstem, synapse directly at the base of OHC and release acetylcholine. A very special type of nicotinic receptor, assembled by α9α10 subunits, participates in this synapse. Here we review recent knowledge and the role of both afferent and efferent synapse in the inner ear.

Keywords: Afferent and efferent synapse; Cochlear hair cells.

Figure 1

Structure of the cochlea and the organ of Corti. A, Cross-section of the cochlea (top inset shows diagram of the whole cochlea and sectioning scheme). The three compartments composing the cochlea are indicated (scala timpani, scala vestibuli and scala media). The organ of Corti is located in the scala media. The spiral ganglion comprises the somas of auditory nerve neurons innervating IHC. B, Structure of the organ of Corti. Inner (1) and outer (2) hair cells are indicated. Afferent dendrites belonging to auditory nerve neurons are indicated in purple, and medial olivary complex neurons in light blue. Some efferent fibers (blue) also make axodendritic contacts with afferent boutons. Som afferent fibers represent a small proportion (type II) of afferent contacts on OHC. Image by Alan Larsen.

Figure 2

Stereocillia and mechano-transduction: A, Scanning electron-micrograph of the surface of the organ of Corti. On the top, the row of IHC stereocillia. The three bottom rows belong to OHC. Scale: 15 µm. Image by Marc Lenoir, INSERM Montpellier, from “Journey into the World of Hearing”, www.cochlea.eu, edu website by Rémy Pujol et al., NeurOreille, Montpellier. B, Mechano-transdcution scheme. In the left diagram, two stereocillia (for simplicity) are illustrated at resting state, connected by a tip link. The tip link is attached to a transduction channel. Deflection of the stereocillia, produced by mechanical force, pulls open the MET channel and activates the current through the channel (as indicated in the text, channels could be located at the bottom of the stereocilia, or even at the top).

Figure 3

Afferent and efferent synapse on hair cells of the cochlea. A, Scheme of the IHC afferent synapse. A postsynaptic bouton of auditory nerve neuron is included (size is overemphasized for illustration purposes). Between 10 to 20 neurons innervate each IHC. A synaptic ribbon is observed opposing to the postsynaptic bouton. An electron-micrograph of the ribbon is shown in detail. Ca²⁺ influx, through voltage-activated calcium channels, is coupled to release of synaptic vesicles. Inset: detail of a synaptic current elicited by the release of a glutamate-filled vesicle/s, and also a synaptic potential followed by an action potential. B, Detailed diagram of the synaptic terminal of MOC neurons onto OHC. MOC terminals release acetylcholine, which activates α9α10 nicotinic receptors in OHCs. Ca²⁺ influx through these receptors activates SK channels. A Ca²⁺ store (included in the diagram) is always observed in direct opposition to the location of the nicotinic receptors. Top inset: typical responses of hair cell to the application acetylcholine. Note the initial and small inward current (carried by the nicotinic receptors) followed the larger outward component due to SK activation. Modified from Taranda et al., 2009.