Morphology of the mammalian vestibulo-ocular reflex: The spatial arrangements of the human fetal semicircular canals and extraocular muscles

The vestibulo-ocular reflex is the system of compensatory ocular movements in response to stimulation of the kinetic labyrinth seen in all vertebrates. It allows maintenance of a stable gaze even when the head is moving. Perhaps the simplest influence on the VOR is the spatial orientation of the planes of the semicircular canals relative to the extraocular muscles. It is hypothesized that the extraocular muscles are in parallel alignment with their corresponding semicircular canals in order to reduce the amount of neural processing needed and hence keep reflex times to a minimum. However, despite its obvious importance, little is known of this spatial arrangement. Moreover, nothing is known about any ontogenetic changes in the relative orientations of the extraocular muscles and semicircular canals. The morphologies of fetal and adult specimens of Homo sapiens were examined using magnetic resonance (MR) images. Three-dimensional co-ordinate data were taken from the images and used to calculate vector equations of the extraocular muscles and planes of best fit for the semicircular canals. The relative orientations of the muscles and canals were then calculated from the vectors and planes. It was shown that there are significant correlations between both the anterior and lateral semicircular canals and their corresponding extraocular muscles during ontogeny. In the case of the lateral canal with the medial rectus, the lateral canal with the lateral rectus, and the anterior canal with the inferior oblique, the trend is towards, though never reaching, alignment, whereas the anterior canal and the superior rectus muscle move out of alignment as age increases. Furthermore, it was noted that none of the six muscle-canal pairs is in perfect alignment, either during ontogeny or in adulthood. It was also shown that the three semicircular canals are not precisely orthogonal, but that the anterior and posterior canals form an angle of about 85 degrees, while the anterior and lateral canals diverge by similar to 100 degrees. Overall, it was shown that there is significant reorientation of the extraocular muscles and semicircular canals during ontogeny, but that, in most cases, there is little realignment beyond the fetal period.