Do agility and skull architecture influence the geometry of the mammalian vestibulo-ocular reflex?

The spatial arrangement of the semicircular canals and extraocular muscles of the eye has been of considerable interest, particularly to researchers working on adaptations of the vestibulo-ocular reflex. Here we offer the first, extensive comparative analysis of the spatial relationships between each extraocular muscle and the canal providing its primary excitatory stimulus. The sample consisted of 113 specimens, representing 51 extant mammalian species. Hypotheses tested included that variations in the spatial alignments are linked with differences of skull morphology and with differences of agility during locomotion. Internal morphologies were visualized with magnetic resonance imaging and were measured with landmark-based vectors and planes. Values for body mass and agility were taken from the existing literature. Data were investigated for trends and associations with standard bivariate and multivariate statistical methods as well as with phylogenetically adjusted bivariate methods. The findings clearly show that species differences in the alignment of each extraocular muscle relative to the canal providing its primary excitatory stimulus are closely associated with changes of orbit morphology. The results also indicate that the actions of the oblique muscles interchange with those of the superior and inferior recti muscles when comparing lateral-eyed (rabbit) with frontal-eyed species (cat). There was only weak evidence to support the notion that canal-muscle alignments differ significantly among species according to how agile they are. The results suggest that semicircular canal morphology is arranged primarily for detecting head movements and then secondarily, if at all, for diminishing the burden of transforming vestibulo-ocular reflex signals in the most agile species.