Neural response directionality correlates of hair cell orientation in a teleost fish

The otolithic end organs in the ears of teleost fishes play important roles in hearing. Although previous studies have shown that afferent fibers innervating otolithic organs are directionally sensitive to acoustic stimulation, no study has demonstrated that directionality of the otolithic afferent neurons derives directly from morphological polarity of the hair cells that they innervate. In this study we investigated whether or not there exists such a structure and function relationship in one of the otolithic organs, the saccule, by using intracellular and extracellular tracing, histochemistry, and confocal imaging techniques. We observed a variety of morphologies of dendritic terminals of saccular ganglion neurons. Arbor innervation areas of these saccular neurons ranged from 893 microm2 to 21,393 microm2, and the number of dendritic endings fell into a range between 10 and 54. We found that the response directionality of saccular ganglion neurons correlates significantly with the morphological polarization of the hair cells in the regions that they innervate. Therefore, we provide direct evidence to support the hypothesis that fish are able to encode directional information about a sound source, particularly in elevation, using arrays of hair cells in the otolithic organs that are oriented specifically along the sound propagation axis.