An Integrated Perspective of Evolution and Development: From Genes to Function to Ear, Lateral Line and Electroreception.

Bernd Fritzsch

doi:10.3390/d13080364

Abstract

Four sensory systems (vestibular, lateral line, electroreception, auditory) are unique and project exclusively to the brainstem of vertebrates. All sensory neurons depend on a common set of genes (Eya1, Sox2, Neurog1, Neurod1) that project to a dorsal nucleus and an intermediate nucleus, which differentiate into the vestibular ear, lateral line and electroreception in vertebrates. In tetrapods, a loss of two sensory systems (lateral line, electroreception) leads to the development of a unique ear and auditory system in amniotes. Lmx1a/b, Gdf7, Wnt1/3a, BMP4/7 and Atoh1 define the lateral line, electroreception and auditory nuclei. In contrast, vestibular nuclei depend on Neurog1/2, Ascl1, Ptf1a and Olig3, among others, to develop an independent origin of the vestibular nuclei. A common origin of hair cells depends on Eya1, Sox2 and Atoh1, which generate the mechanosensory cells. Several proteins define the polarity of hair cells in the ear and lateral line. A unique connection of stereocilia requires CDH23 and PCDH15 for connections and TMC1/2 proteins to perceive mechanosensory input. Electroreception has no polarity, and a different system is used to drive electroreceptors. All hair cells function by excitation via ribbons to activate neurons that innervate the distinct target areas. An integrated perspective is presented to understand the gain and loss of different sensory systems.

Highlights

Sensory maps depend on the specific sensory modality and the relevant information to be extracted by them
The evolution of chordates is comparable with the organization of the dorsal spinal cord and brainstem, which is associated with neurons and hair cells in 71,000 vertebrates
Apical kinocilia surrounded by microvilli resemble the electroreceptor hair cells, having either a central kinocilium or microvilli [22,23,27]

Summary

Introduction

Sensory maps depend on the specific sensory modality and the relevant information to be extracted by them. The vestibular, lateral line, electroreception and cochlea independently reach hair cells that form prior to neurons [23,136], consistent with the same pattern of neurons that develop first, followed by the central axon to the brainstem, and later followed by the hair cell innervation [3,109,134,137]. This is obvious in cases where hair cells are not formed, such as in Atoh null mice, which show a near-normal central projection [131,138]. Some central topology found in some, but not all, lateral line and electroreceptors, show an incomplete segregation for the vestibular neurons

The Brainstem Is Transformed from the Spinal Cord

Conclusions