The generation of compensatory eye movements in response to rotational head movements involves the transformation of visual-optokinetic and vestibular signals into commands controlling the appropriate eye muscles. Previously, it has been shown that the three systems (optokinetic, vestibular, and eye muscle) share a similar three-dimensional reference frame. In this report, we suggest that a peculiarity in the structure of the horizontal recti in pigeons demonstrates that the optokinetic system is organized with respect to the eye muscles rather than the vestibular canals. Measurements of the orientation of the plane for each of the lateral and medial recti were obtained. These were compared with the direction preferences of optokinetic neurons responsive to horizontal motion, namely “back” units in the nucleus of the basal optic root (nBOR), “forward” units in the pretectal nucleus lentiformis mesencephali (LM), and “vertical axis” (VA) Purkinje cells in the flocculus. The average direction preference of LM neurons excited in response to forward (temporal to nasal) visual motion, and VA Purkinje cells in response to optokinetic motion in the ipsilateral visual field was approximately parallel to the visual horizontal. This corresponded to the orientation of the medial rectus, which was also approximately parallel to the visual horizontal. The average direction preference of nBOR neurons excited in response to backward (nasal to temporal) visual motion, and VA Purkinje cells in response to optokinetic motion in the contralateral visual field was approximately 20–30 deg down from the visual horizontal. The orientation of the lateral rectus was also approximately 20–30 deg down from the visual horizontal. These data suggest that the incoming optokinetic signals are organized with respect to the outgoing extraocular muscle commands.