Development and evolution of inner ear sensory epithelia and their innervation

Abstract

ABSTRACT:The development and evolution of the inner ear sensory patches and their innervation is reviewed. Recent molecular developmental data suggest that development of these sensory patches is a developmental recapitulation of the evolutionary history. These data suggest that the ear generates multiple, functionally diverse sensory epithelia by dividing a single sensory primordium. Those epithelia will establish distinct identities through the overlapping expression of genes of which only a few are currently known. One of these distinctions is the unique pattern of hair cell polarity. A hypothesis is presented on how the hair cell polarity may relate to the progressive segregation of the six sensory epithelia. Besides being markers for sensory epithelia development, neurotrophins are also expressed in delaminating cells that migrate toward the developing vestibular and cochlear ganglia. These delaminating cells originate from multiple sites at or near the developing sensory epithelia and some also express neuronal markers such as NeuroD. The differential origin of precursors raises the possibility that some sensory neurons acquire positional information before they delaminate the ear. Such an identity of these delaminating sensory neurons may be used both to navigate their dendrites to the area they delaminated from, as well as to help them navigate to their central target. The navigational properties of sensory neurons as well as the acquisition of discrete sensory patch phenotypes implies a much more sophisticated subdivision of the developing otocyst than the few available gene expression studies suggest.

Expression of prestin-homologous solute carrier (SLC26) in auditory organs of nonmammalian vertebrates and insects

“…Evolutionarily, the auditory organs of teleost fish (sacculus and lagena) and mammals (cochlea) can be traced back to a single evolutionary origin (30). With an amino acid sequence identity of 49.8%, Zebrafish I is closer to rat prestin than any other known member of the mammalian SLC26 family (rat pendrin, 36.4% identity).…”

Molecular Conservation and Novelties in Vertebrate Ear Development

“…As previously pointed out by Carney and Silver (1983) and recently confirmed (Farinas et al, 2001;Fritzsch et al, 2002), delaminating cells (which are likely neuronal precursors based on Neurod1 expression) apparently migrate away from the otocyst along fibers of more differentiated neurons that project toward the future sensory epithelia. Indeed, it appears that spatiotemporally distinct populations of primary sensory neuron precursors specifically extend along the existing neuronal fibers that reach toward the future primary sensory epithelium.…”

“…There is now uniform agreement that the auditory part of the ear evolved from vestibular organs (Fritzsch, 1999;Wever, 1974). For example, it is likely that the auditory organ of the mammalian ear, the cochlea, evolved through the embryonic transformation of parts of the saccule (Fritzsch, 1992;Fritzsch et al, 2002). In contrast to this universally accepted idea of evolutionary transformation of a vestibular organ into an auditory organ, there is no agreement on the evolution of the vestibular part of the ear.…”

“…Primary neuron primordia can be identified either as delaminating cells (Carney and Silver, 1983;Farinas et al, 2001;Fritzsch et al, 2002) emigrating through the basal lamina surrounding the otocyst or as cells that express specific markers such as Ngn1 (Ma et al, 1998), NeuroD (Kim et al, 2001;Liu et al, 2000), neurotrophins (Farinas et al, 2001), or other genes (Fekete and Wu, 2002). Such delaminating cells are first apparent shortly after the otocyst closes in mouse (E9.5) or even before the otocyst is completely formed in chicken (Adam et al, 1998).…”

“…In general, neurosensory evolution of the ear is based on the multiplication of existing sensory patches and their innervation (Fritzsch and Wake, 1988;Fritzsch et al, 2002). These modifications are likely followed by functional diversification through creation of modified, unique acellular covering structures (Goodyear and Richardson, 2002) that allow transduction of a previously unexplored property of the mechanical energy that reaches the ear.…”