V. THE INNER EAR: GENERAL PROPERTIES OF RECEPTORS

The membranous labyrinth consists of endolymph-filled vesicles and canals in communication with each other. These vesicles and canals have thin transparent walls which are composed of a connective membrane of mesenchymal origin and are lined on the inner side with an epithelium of ectodermal origin. Within the membranous labyrinth there are six specialized receptor organs within which are found modified sensory epithelial cells. One of these specialized area, called the organ of Corti, is specialized to transduce sound; the remaining five, the maculae of the utricle and saccule and cristae of the three semicircular canals, are sensitive to head position or head movement. Figure V-1 illustrates the general layout of the inner ear.

While the structure of receptor organs in the cochlea and the vestibular labyrinth exhibit structural specialization that provides selectivity to a particular sensory input, their general characteristics and functional properties are very similar. For each of the six receptor organs of the inner ear we can make the following statements:

1. The receptor cells are modified epithelial cells. Such a cell is cylindrical or flask-shaped and is equipped at its apical end with a bundle of sensory hairs called stereocilia. Often found located adjacent the stereocilia is a single kinocilium, or true cilium. The presence of sensory hairs gives these cells their name: hair cells.

2. The hair cells are held in position by a system of supporting cells.

3. Each receptor organ is equipped with an auxiliary structure with which the stereocilia of the hair cells come into contact. Movement of the auxiliary structure relative to the hairs displaces the cilia, and this displacement is the adequate stimulus for activating the hair cell.

4. Each hair cell is innervated at its base by afferent endings of sensory nerve fibers and by one or several endings of efferent centrifugal nerve fibers. Synaptic contact between hair cell and nerve fiber is chemical in nature, although the identity of the neurotransmitter(s) involved has not be made. In the organ of Corti the sensory cells are innervated by the fibers of the cochlear nerve; in the maculae of the saccule and utricle and the cristae ampullae they are innervated by the fibers of the vestibular nerve.

Hair cells of the inner ear are epithelial cells which, in the vertebrate embryo, originate from the surface ectoderm and not from the neural tube that forms the central nervous system. Hair cells all morphologically similar. Figure V-2 illustrates schematically the major structural features of a hair cell.

The cell is cylindrical or flask-shaped and is equipped at its apical end with a bundle of sensory hairs called stereocilia. Hair bundles occur in a variety of sizes and shapes and, for any given hair cell, may vary in number. As a rule, stereocilia uniformly lie in a hexagonal array and increase in length from one edge of the hair bundle to the other (Figure V-3).  A single kinocilium is present, which differs in structure from stereocilia and which is asymmetrically placed at one edge of the stereocilial bundle, usually adjacent to the tallest of these (in the  cochlea the kinocilium is present in early development but is absent in the adult). The kinocilium is associated with an intracellular organelle, the basal body. This orientation of hair cells with respect to the kinocilium is referred to as morphological polarization. Morphological polarization is related to the directional sensitivity of the hair cell.

In the receptor organ, hair cells rest on a basal lamina and are joined to one another by tight junctions.   As epithelial cells, they lack axons and dendrites. Instead, hair cells make synapses onto afferent nerve fibers of the eighth cranial nerve and also receive efferent synaptic contacts from axons originating in the brainstem. Thus, the neural mechanisms that underlie excitation and sensory processing in the cochlea and vestibular labyrinth are unlike those of most other mechanoreceptor nerve preparations (e.g., Pacinian corpuscle) in that the receptor is NOT part of the sensory neuron but is a specialized epithelial cell which excites the sensory neuron by synaptic transmission.

Stereocilia consist of actin filaments within a tubular membrane. Because the filaments are crossbridged, each stereocilium behaves like a stiff rod which pivots at its base. The adequate stimulus for the hair cell is displacement of the hair bundle.  The hair cell is a mechanoreceptor, producing an electrical signal, or receptor potential, in response to mechanical stimulation of its hair bundle. It is the relative motion between the hair cell and the auxiliary structure specific to the receptor organ that provides the displacement.

Hair cells are extraordinarily sensitive to cilia displacement. If the height of one cilium is scaled to the height of Chicago's Sear's Tower, the movement of the tip of the cilium at the threshold of hearing is equivalent to a two-inch displacement of the top of the Tower (Figure V-4)! At threshold detection levels in humans, the auditory or the vestibular systems are operating at the same order of magnitude of displacement as that of thermal motion.

Although it has been possible to learn a considerable amount about the operation of hair cells in the mammalian inner ear, a more nearly complete picture of the transduction process has emerged from in vitro studies of hair cells from lower vertebrates. Under these conditions it is possible to insert a glass microelectrode into a hair cell and thereby record the intracellular electrical events when the hair bundle is deflected. In a quiescent cell, the resting membrane potential is around 60 mv.

As in the case in neurons, the electrical signals in the hair cell originate from the flow of ionic currents across the membrane through specific pores, or ion channels. The identity of ion channels and their kinetics is studied electrophysiologically using 'patch clamp' techniques. Movement of the hair bundle in the depolarizing direction leads to increases in membrane conductance, meaning that the membrane becomes more permeable to positively charged ions. It is now believed that the ion channels admitting positively charge ions during positive deflection, the transduction channels, are located at the tips of the stereocilia. These are opened by a mechanical linkage that exists between adjacent hairs of the hair bundle. Movement in the opposite direction closes channels thereby stemming the flow of ionic current. Additional ion channels with different specificity and function are located on the cell body and in the synaptic region. It is known that amino glycosides, such as occur in certain ototoxic antibiotics, interfere with channel operation. Also, very loud sound may physically disrupt the bundle structure. Thus, interfering with ion-channel operations or changing the physical arrangement of the stereocilia is sufficient to alter mechanoelectrical transduction in the inner ear.