Three-dimensional extraocular motoneuron innervation in the rhesus monkey - I: Muscle rotation axes and on-directions during fixation

The rotation axis for each of the six extraocular muscles was determined in four eyes from three perfused rhesus monkeys. Measurements of the location s of muscle insertions and origins were made in the stereotaxic reference f rame with the x-y plane horizontal and the x-z plane sagittal. The computed rotation axes of the horizontal recti were close to being in the x-z plane at an angle of about 15 degrees to the z axis. The rotation axes of the ve rtical recti and the obliques were close to being in the x-y plane at an an gle of about 30 degrees to the y axis. In five alert rhesus monkeys, we sim ultaneously recorded extraocular motoneuron activity and eye position in th ree dimensions (3D). The activity of 51 motoneuron axons was obtained from the oculomotor (n=34), trochlear (n=11), and abducens nerve (n=6) during sp ontaneous eye movements. To extend the torsional range of eye position, the animals were also put in different static roll positions, which induced oc ular counter-roll without dynamic vestibular stimulation. Periods of 100 ms during fixation or slow eye movements (<10 degrees/s) were chosen for anal ysis. For each motoneuron, a multiple linear regression was performed betwe en firing frequency and 3D eye position, expressed as a rotation vector, in both stereotaxic and Listing's reference frame. The direction with the hig hest correlation coefficient (average R=0.94+/-0.07 SD) was taken as the on -direction. Each unit's activity could be unequivocally attributed to one p articular muscle. On-directions for each motoneuron were confined to a well -defined cone in 3D. Average on-directions of motoneurons differed signific antly from the corresponding anatomically determined muscle rotation axes e xpressed in the stereotaxic reference frame (range of deviations: 11.9 degr ees to 29.0 degrees). This difference was most pronounced for the vertical recti and oblique muscles. The muscle rotation axes of the vertical rectus pair and the oblique muscle pair form an angle of 58.3 degrees, whereas the corresponding angle for paired motoneuron on-directions was 105.6 degrees. On-directions of motoneurons were better aligned with the on-directions of semicircular canal afferents (range of deviation: 9.4-18.9 degrees) or wit h the anatomically determined sensitivity vectors of the semicircular canal s (range of deviation: 3.9-15.9 degrees) than with the anatomically determi ned muscle rotation axes, but significant differences remain to be explaine d. The on-directions of motoneurons were arranged symmetrically to Listing' s plane, in the sense that the torsional components for antagonistically pa ired muscles were almost equal, but of opposite sign. Thus, the torsional c omponents of motoneuron on-directions cancel when eye movements are confine d to Listing's plane. This arrangement simplifies the neuronal transformati ons for conjugate head-fixed voluntary eye movements, while the approximate alignment with the semicircular canal reference frame is optimal for gener ating compensatory eye movements.