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 muscl
es. Previously, it has been shown that the three systems (optokinetic,
vestibular, and eye muscle) share a similar three-dimensional referen
ce frame. In this report, we suggest that a peculiarity in the structu
re of the horizontal recti in pigeons demonstrates that the optokineti
c system is organized with respect to the eye muscles rather than the
vestibular canals. Measurements of the orientation of the plane for ea
ch of the lateral and medial recti were obtained. These were compared
with the direction preferences of optokinetic neurons responsive to ho
rizontal motion, namely ''back'' units in the nucleus of the basal opt
ic root (nBOR), ''forward'' units in the pretectal nucleus lentiformis
mesencephali (LM), and ''vertical axis'' (VA) Purkinje cells in the f
locculus. The average direction preference of LM neurons excited in re
sponse to forward (temporal to nasal) visual motion, and VA Purkinje c
ells in response to optokinetic motion in the ipsilateral visual field
was approximately parallel to the visual horizontal. This corresponde
d to the orientation of the medial rectus, which was also approximatel
y parallel to the visual horizontal. The average direction preference
of nBOR neurons excited in response to backward (nasal to temporal) vi
sual motion, and VA Purkinje cells in response to optokinetic motion i
n 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 s
uggest that the incoming optokinetic signals are organized with respec
t to the outgoing extraocular muscle commands.