Connecting Ears to Eye Muscles: Evolution of a ‘Simple' Reflex Arc

Abstract

Developmental and evolutionary data from vertebrates are beginning to elucidate the origin of the sensorimotor pathway that links gravity and motion detection to image-stabilizing eye movements - the vestibulo-ocular reflex (VOR). Conserved transcription factors coordinate the development of the vertebrate ear into three functional sensory compartments (graviception/translational linear acceleration, angular acceleration and sound perception). These sensory components connect to specific populations of vestibular and auditory projection neurons in the dorsal hindbrain through undetermined molecular mechanisms. In contrast, a molecular basis for the patterning of the vestibular projection neurons is beginning to emerge. These are organized through the actions of rostrocaudally and dorsoventrally restricted transcription factors into a ‘hodological mosaic' within which coherent and largely segregated subgroups are specified to project to different targets in the spinal cord and brain stem. A specific set of these regionally diverse vestibular projection neurons functions as the central element that transforms vestibular sensory signals generated by active and passive head and body movements into motor output through the extraocular muscles. The large dynamic range of motion-related sensory signals requires an organization of VOR pathways as parallel, frequency-tuned, hierarchical connections from the sensory periphery to the motor output. We suggest that eyes, ears and functional connections subserving the VOR are vertebrate novelties that evolved into a functionally coherent motor control system in an almost stereotypic organization across vertebrate taxa.

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

“…The distribution of vestibular subgroups with projections to spatially specific sets of extraocular motoneurons in separate rhombomeric compartments complies with a processing of head/body motion signals within a motor map that likely also includes vestibulo-spinal neurons for posture and locomotor control (left scheme in Fig. 4C) [Straka and Baker 2013; Straka et al 2014]. As will be shown in the next section, this is at variance with the lateral line system, where signals related to water motion are processed within a sensory map.…”

“…The first of these inventions is the set of epidermal placodes that are present only in craniate chordates [Northcutt and Gans 1983]. In addition to placodes associated with gustatory [Iskusnykh et al 2016; Qian et al 2001], paratympanic and spiracular organs [O’Neill et al 2012], regionally localized placodes give rise to lateral line, electroreceptive and vestibular/auditory neurons, which project to specific nuclear areas in the dorsolateral part of the hindbrain [Dabdoub et al 2016; Straka et al 2014]. The evolutionary origin of these placodes is not clear.…”

“…Vestibular afferents that supply all inner ear endorgans join into a single nerve [Straka et al 2014] that splits after entering the hindbrain into an ascending and descending fiber bundle [Birinyi et al 2001]. While afferent fibers from different mechanosensory modalities terminate in non-overlapping central areas, afferent projections from different vestibular sensory endorgans overlap extensively within their dedicated hindbrain recipient nuclei (Fig.…”

“…In contrast, semicircular canal and utricular/lagenar afferents occupy the same dorso-lateral hindbrain area without any evidence for an endorgan-related topographical segregation (Fig. 4B) [Straka et al 2014]. In addition, vestibular afferents project into the cerebellum and in an endorgan-specific manner (horizontal semicircular canal and utricular afferents) into the r5/r6 reticular formation [Birinyi et al 2001; Will et al 1985].…”

“…In addition, vestibular afferents project into the cerebellum and in an endorgan-specific manner (horizontal semicircular canal and utricular afferents) into the r5/r6 reticular formation [Birinyi et al 2001; Will et al 1985]. In the vestibular nuclei, afferent nerve projections from different semicircular canals and otolith organs as well as afferent fibers with different diameters and thus with different response dynamics overlap to a considerable extent within the termination area [Straka and Dieringer 2004; Straka et al 2014]. The absence of endorgan-specific regionally restricted terminal zones, comparable to the retinotopic projections of the visual system, suggests that vestibular signals are not sorted in the CNS based on a sensory topography.…”