Control of Vertical Gaze in the Midbrain

A rostral portion of the midbrain reticular formation adjacent to the periaqueductal gray (riMLF) contains neurons whose primary on-directions are related to vertical gaze (combined head and eye movements), as do regions near the interstitial nucleus of Cajal (Fig. 1C). These burst neurons (both excitatory and inhibitory) fire during every vertical or torsional saccadic eye movement as well as during the quick phases of vertical, vestibularly induced nystagmus. Efferent projections from the riMLF synapse in, but also pass through and lateral to, the interstitial nucleus of Cajal (Fig. 7). As a result, electrolytic lesions or ischemic insult to the interstitial nucleus destroys the output of the riMLF as well as that ofthe neurons in the nucleus. This probably accounts for the long-held view that the interstitial nucleus of Cajal rather than the riMLF was the premotor center for coordinating vertical gaze. Instead, the cells in the interstitial nucleus produce a prolonged step of activity in response to every vertical rapid eye movement. This suggests that the interstitial nucleus is a critical structure for vertical gaze holding. In this way, it serves the same function for the vertical oculomotor system that the nucleus prepositus hypo-glossus does for the horizontal eye movement system.

The projections from the riMLF and interstitial nucleus to the oculomotor nuclei account for the ability of these structures to generate vertical eye movements (Fig. 7). During downward movements, the riMLFs on both sides of the midbrain must be

Saccadic Pathway Diagram
Figure 7 Schematic diagram of the final common pathway for vertical saccades. X marks the location of a cut in the posterior commissure (PC) that would produce the dorsal midbrain syndrome (see Table II). See Table I.

active. Projections from one riMLF reach the riMLF on the opposite side. There are direct projections from the riMLF to the inferior rectus and superior oblique motoneurons on the ipsilateral side. This produces a downward movement of both eyes (i.e., inferior rectus on the same side and the axons of the trochlear motoneurons cross the brain stem to reach the contralateral superior oblique muscle, which causes the opposite eye to be depressed and intorted). To coordinate upward movements, the riMLF provides efferent projections that synapse on the motoneurons in the superior rectus and inferior oblique subdivisions of the oculomotor complex on both sides. Similar to the efferent projections of the riMLF, the output of the interstitial nucleus is directed to the motoneurons of the oculomotor and trochlear nuclei as well as to the contralateral interstitial nucleus.

Inactivation experiments of the riMLF unilaterally demonstrated a 50% reduction in conjugate vertical eye velocity and a complete loss of one torsional direction. Clockwise (CW) rotation disappeared when the right riMLF was inactivated, whereas after inactivation of the left riMLF counterclockwise (CCW) torsion disappeared. Interestingly, changes in horizontal movements also occurred, suggesting that the short-lead burst neurons of the riMLF are divided into four groups: CW-up-left and CW-down-right in the right riMLF and CCW-up-right and CCW-down-left in the left riMLF. Bilateral inactivation led to complete abolition of both torsional and vertical saccadic eye movements. Unilateral inactivation or destruction (with kainic acid) led to similar modifications of torsional eye movements and a shift in Listing's plane. Clinical material supports the idea that the riMLF is the region equivalent to the paramedian pontine reticular formation (where horizontal movements are coordinated) for the coordination of eye movements in the vertical plane (see later discussion). On the other hand, unilateral inactivation of the interstitial nucleus of Cajal led to the loss of vertical gaze holding, skew deviation with hypertropia of the ipsilateral eye, extorsion of the contralateral eye, intorsion of the ipsilateral eye, and a contralateral head tilt (ocular tilt reaction). This confirmed the important role that the interstitial nucleus plays in maintaining vertical gaze positions. Similar to the discussion found on horizontal gaze, the separation of signals for the generation of vertical movements must occur as projections reach the riMLF. However, the same analysis of long-lead burst neurons found in the PPRF has not occurred for the vertical long-lead bursters. Finally, whereas projections from the superior colliculus, nucleus of the posterior commissure, long-lead burst neurons of the midbrain, and pontine reticular formations to the riMLF have been described, no direct projections from the frontal eye fields to the riMLF have been identified. This has suggested that cortical supranuclear control of vertical eye movements may be mediated through the nuclei of the posterior commissure, which receive a strong frontal eye field projection.

D. Clinical Correlation: Localization of Up and Down Gaze in the Midbrain

Experimental material and clinical cases agree that damage to the posterior commissure produces a paralysis of up gaze and a variety of associated

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