Spatial coordination of compensatory eye movements in vertebrates: form and function.

The semicircular canals of the labyrinth of vertebrates provide one way of motion detection in three-dimensional space. The fully developed form of the vertebrate labyrinth consists of six semicircular canals, three on each side of the head, whose spatial arrangement (vertical canals are placed diagonally in the head, horizontal canals are oriented earth horizontally) follows three interconnected principles: 1) bilateral symmetry, 2) push-pull operational mode, and 3) mutual orthogonality. Other sensory and motor systems related to vestibular reflexes, such as the extraocular muscles or the "optokinetic" coordinate axes encoded in the activity of the visually driven cells of the accessory optic system, share the same geometrical framework. This framework is also reflected in the anatomical networks mediating compensatory eye movements, linking each of the semicircular canals to a particular set of extraocular muscles (so-called principal vestibuloocular reflex connections to yoke muscles). These classical vestibulo-oculomotor relationships have been verified at many levels of the vertebrate hierarchy, including lateral- and frontal-eyed animals. The particular spatial orientation of the semicircular canals requires further comment and phylogenetic evaluation. The spatial arrangement of the vertical canals is already present in fossil ostracoderms, and is also exemplified in lampreys, the modern forms of once abundant agnathan species that populated the Silurian and Devonian oceans. The lampreys and ostracoderms lack horizontal canals, which appear later in all descendent vertebrates. The fully developed vertebrate labyrinth with its six semicircular canals displays distinct differences that are obvious when comparing distant taxa (e.g. elasmobranchs versus other vertebrates). Whereas the common crus of the semicircular canals in teleosts through mammals is formed between the anterior and the posterior semicircular canal, it occurs between the anterior and the horizontal canal in elasmobranchs. However, despite this morphological difference, these two vertebrate labyrinth prototypes constitute a functionally identical solution. A similar analysis holds for certain invertebrate species (crab, octopus, squid), which display an even wider variety in the physical expressions of movement detection systems when compared to vertebrates. Although the physical expressions of motion detection systems differ in the animal kingdom, the functional solutions (providing the best signal-to-noise ratio) with adherence to bilateral symmetry, push-pull operational mode, and mutual orthogonality are identical.(ABSTRACT TRUNCATED AT 400 WORDS)