Cerebellum and ocular motor control

Abstract

An intact cerebellum is a prerequisite for optimal ocular motor performance. The cerebellum fine-tunes each of the subtypes of eye movements so they work together to bring and maintain images of objects of interest on the fovea. Here we review the major aspects of the contribution of the cerebellum to ocular motor control. The approach will be based on structural-functional correlation, combining the effects of lesions and the results from physiologic studies, with the emphasis on the cerebellar regions known to be most closely related to ocular motor function: (1) the flocculus/paraflocculus for high-frequency (brief) vestibular responses, sustained pursuit eye movements, and gaze holding, (2) the nodulus/ventral uvula for low-frequency (sustained) vestibular responses, and (3) the dorsal oculomotor vermis and its target in the posterior portion of the fastigial nucleus (the fastigial oculomotor region) for saccades and pursuit initiation.

Keywords: fastigial; flocculus; nodulus; paraflocculus; pursuit; saccade; vermis; vestibular.

Figure 1

Cerebellar structures important for eye movement control: (A) sagittal view (B) inferior view (modified after Leigh and Zee, 2006).

Figure 2

Flocculus improves neural integrator function by a positive feedback loop (“k”). An inherently poor gaze-holding network resides in the brain stem. By virtue of positive feedback, the flocculus can modulate the ability of the brain stem neural integrator to generate a steady tonic eye position command. If feedback is inadequate, gaze holding is impaired. If feedback is excessive, gaze is unstable (Zee et al., 1981).

Figure 3

Increased VOR gain with cerebellar disease. The inverse of horizontal eye position (black trace) is superimposed on the head position (gray trace) while the patient is fixating on a target during sinusoidal head rotation. Frequent corrective, back up saccades (black arrow) are required to stay on the target and compensate for increased VOR gain.

Figure 4

Position plots of representative yaw impulse responses in a normal subject and a patient with cerebellar disease. Horizontal and vertical head (inverted) and eye-in-head positions are shown for rightward yaw impulses, starting from the center position. For the patient, the change in horizontal eye position exceeds the change in head position (i.e., the gain is high). At the same time, the eye moves up in the orbit, even though there is essentially no downward head movement. The arrows indicate horizontal and vertical components of a saccade that partially corrects the gaze position error. Right-hand-rule conventions are used: positive positions are leftward and downward, except for head positions, which are inverted to facilitate comparison (reprinted from Walker and Zee (2005a), with permission from the American Physiologic Society).

Figure 5

Some major structures and their main connections are shown for saccade control in one direction. During the saccade, the cerebellum integrates the efference copy of the drive signal from the NRTP (ipsilateral to the movement) that projects bilaterally to both OMV and FOR within the cerebellum. The SC and the FOR (both contralateral to the movement) excite the EBN that contact the motoneurons (both ipsilateral to the movement) of the agonist muscle. When the eyes approach the target, the ipsilateral FOR neurons produce a choke signal through the contralateral IBN that inhibits the motoneurons of the agonist muscle. NRTP, nucleus reticularis tegmenti pontis; DLPN, dorsolateral pontine nuclei; OMV, oculomotor vermis; FOR, fastigial oculomotor region; SC, superior colliculus; EBN, excitatory burst neurons; IBN, inhibitory burst neurons (modified after Quaia et al., 1999).

Figure 6

Some smooth pursuit-related structures and their major projections. The brain stem afferents form the DLPN project more strongly to the flocculus/paraflocculus and the NRTP afferents mainly terminate in the OMV region. Cerebellar output from the flocculus/paraflocculus to the ocular motoneurons relays through the MVN whereas the projections from the OMV/FOR are not known. NRTP, nucleus reticularis tegmenti pontis; DLPN, dorsolateral pontine nuclei; OMV, oculomotor vermis; FOR, fastigial oculomotor region; MVN, medial vestibular nucleus.