Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective

Abstract

Detection of motion is a feature essential to any living animal. In vertebrates, mechanosensory hair cells organized into the lateral line and vestibular systems are used to detect external water or head/body motion, respectively. While the neuronal components to detect these physical attributes are similar between the two sensory systems, the organizational pattern of the receptors in the periphery and the distribution of hindbrain afferent and efferent projections are adapted to the specific functions of the respective system. Here we provide a concise review comparing the functional organization of the vestibular and lateral line systems from the development of the organs to the wiring from the periphery and the first processing stages. The goal of this review is to highlight the similarities and differences to demonstrate how evolution caused a common neuronal substrate to adapt to different functions, one for the detection of external water stimuli and the generation of sensory maps and the other for the detection of self-motion and the generation of motor commands for immediate behavioral reactions.

Synaptic convergence of afferent inputs in primary infrared-sensitive nucleus (LTTD) neurons of rattlesnakes (Crotalinae) as the origin for sensory contrast enhancement

“…The distinct spatial pattern of electrically activated synaptic responses within the morphological limits of the LTTD complies with the region-specific termination of pit organ-innervating trigeminal afferents (Kohl et al, 2014). Accordingly, IR signals form a sensory map along the rostro-caudal extent of the hindbrain comparable to, for example, visual signals within the optic tectum (Dräger and Hubel, 1976;Heric and Kruger, 1965;Stanford and Hartline, 1984) rather than a motor map such as for vestibular signals in the adjacent hindbrain area (Chagnaud et al, 2017). Major hallmark features of the region-specific central IR object representation are complex, yet dynamically structured synaptic responses that derive from predictable combinations of EPSPs and IPSPs in compliance with results from previous extracellular recordings (Stanford and Hartline, 1984).…”

Ear transplantations reveal conservation of inner ear afferent pathfinding cues

“…Inner ear sensory neurons are derived from the otic placode and make stereotyped connections with both inner ear hair cells at the periphery and second order central neuron targets in the hindbrain 1 – 3 . These neurons transmit vestibular and auditory information to the appropriate second order neurons in the hindbrain for normal function 4 . Within the hindbrain, inner ear auditory and vestibular sensory afferents project directly to the auditory and vestibular nuclei, respectively 5 , 6 .…”

“…Both Prickle1 and Wnt signaling receptors (Frizzled receptors) are regulated by Neurod1 23 , known to affect dorsoventral patterning of inner ear afferents 21 . Since inner ear afferents project to the same dorsoventral location within the hindbrains across all vertebrates 4 , 18 , we assume that all neural crest and placode derived cranial nerve afferents are navigating in the hindbrain using a conserved set of guidance molecules. Given the conservation of transcription factors and expression of diffusible molecules, such as Wnt, BMP, and Shh, across species and between the hindbrain and spinal cord 24 , 25 , we used a novel approach to investigate whether presumed conserved guidance molecules may play a role in the initial targeting of inner ear afferents through heterochronic, xenoplastic, and heterotopic transplantations in chickens and mice.…”

Conserved and divergent development of brainstem vestibuloacoustic nuclei

“…Vestibular peripheral organs, hindbrain vestibular nuclei and their connectivity patterns are highly conserved across vertebrates and clear evolutionary relationships can be established (Straka and Baker, 2013). The axial developmental origin and location of vestibular neurons projecting to oculomotor, spinal cord, cerebellar and commissural targets are also conserved (Branoner et al, 2016;Chagnaud et al, 2017;Malinvaud et al, 2010;Straka and Baker, 2013;Straka et al, 2014), however, a comparative analysis of the dorsoventral lineage of hindbrain vestibular neurons has been lacking. Here, we show that in chick, cells derived from rhombic lip Atoh1 + progenitors are present in the Superior, Deiters, Medial and Descending vestibular nuclei, while we observed no contribution from this lineage to the avian exclusive Tangential nucleus (Figures 5 and 6).…”