Abstract
All craniate chordates have inner ears with hair cells that receive input from the brain by cholinergic centrifugal fibers, the so-called inner ear efferents (IEEs). Comparative data suggest that IEEs derive from facial branchial motor (FBM) neurons that project to the inner ear instead of facial muscles. Developmental data showed that IEEs develop adjacent to FBMs and segregation from IEEs might depend on few transcription factors uniquely associated with IEEs. Like other cholinergic terminals in the peripheral nervous system (PNS), efferent terminals signal on hair cells through nicotinic acetylcholine channels, likely composed out of alpha 9 and alpha 10 units (Chrna9, Chrna10). Consistent with the evolutionary ancestry of IEEs is the even more conserved ancestry of Chrna9 and 10. The evolutionary appearance of IEEs may reflect access of FBMs to a novel target, possibly related to displacement or loss of mesoderm-derived muscle fibers by the ectoderm-derived ear vesicle. Experimental transplantations mimicking this possible aspect of ear evolution showed that different motor neurons of the spinal cord or brainstem form cholinergic synapses on hair cells when ears replace somites or eyes. Transplantation provides experimental evidence in support of the evolutionary switch of FBM neurons to become IEEs. Mammals uniquely evolved a prestin related motor system to cause shape changes in outer hair cells regulated by the IEEs. In summary, an ancient motor neuron population drives in craniates via signaling through highly conserved Chrna receptors a uniquely derived cellular contractility system that is essential for hearing in mammals.
Highlights
The central nervous system (CNS) of craniate chordates connects to peripheral target organs via two sets of nerve fibers comprising the peripheral nervous system (PNS): 1) Afferent fibers bring information into the CNS
Central axons end in the alar plate of the spinal cord and hindbrain whereas the distal processes contact skin and muscle associated receptors and inner ear, lateral line, and taste bud sensory cells
In contrast to the visual system, the highly divergent original findings on the inner ear efferent (IEE) system (Fritzsch et al, 2016a) soon concentrated on a single theme: efferents to the ear being evolutionary derived from facial branchial motor neurons (FBMs) (Roberts and Meredith, 1992; Sienknecht et al, 2014)
Summary
The central nervous system (CNS) of craniate chordates connects to peripheral target organs via two sets of nerve fibers comprising the peripheral nervous system (PNS): 1) Afferent (centripetal) fibers bring information into the CNS. In contrast to the visual system, the highly divergent original findings on the inner ear efferent (IEE) system (Fritzsch et al, 2016a) soon concentrated on a single theme: efferents to the ear being evolutionary derived from facial branchial motor neurons (FBMs) (Roberts and Meredith, 1992; Sienknecht et al, 2014).
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