Multispectral four-dimensional imaging reveals that evoked activity modulates peripheral arborization and the selection of plane-polarized targets by sensory neurons

Abstract

The polarity of apical stereocilia endows hair cells with directional excitability, which in turn enables animals to determine the vectorial component of a sound. Neuromasts of the lateral line of aquatic vertebrates harbor two populations of hair cells that are oriented at 180° relative to each other. The resulting sensory-vectorial ambiguity is solved by lateralis afferent neurons that discriminate between hair cells of opposite polarities to innervate only those with the same orientation. How neurons select identically oriented hair cells remains unknown. To gain insight into the mechanism that underlies this selection, we devised a simple method to gather dynamic morphometric information about axonal terminals in toto by four-dimensional imaging. Applying this strategy to the zebrafish allowed us to correlate hair cell orientation to single afferent neurons at subcellular resolution. Here we show that in zebrafish with absent hair cell mechanoreception, lateralis afferents arborize profusely in the periphery, display less stability, and make improper target selections. Central axons, however, show no dynamic changes and establish normal contacts with the Mauthner cell, a characteristic second-order target in the hindbrain. We propose that the hardwired developmental mechanisms that underlie peripheral arborization and target recognition are modulated by evoked hair cell activity. This interplay between intrinsic and extrinsic cues is essential for plane-polarized target selection by lateralis afferent neurons.