A central mesencephalic reticular formation projection to medial rectus motoneurons supplying singly and multiply innervated extraocular muscle fibers

Abstract

We recently demonstrated a bilateral projection to the supraoculomotor area from the central mesencephalic reticular formation (cMRF), a region implicated in horizontal gaze changes. C-group motoneurons, which supply multiply innervated fibers in the medial rectus muscle, are located within the primate supraoculomotor area, but their inputs and function are poorly understood. Here, we tested whether C-group motoneurons in Macaca fascicularis monkeys receive a direct cMRF input by injecting this portion of the reticular formation with anterograde tracers in combination with injection of retrograde tracer into the medial rectus muscle. The results indicate that the cMRF provides a dense, bilateral projection to the region of the medial rectus C-group motoneurons. Numerous close associations between labeled terminals and each multiply innervated fiber motoneuron were present. Within the oculomotor nucleus, a much sparser ipsilateral projection onto some of the A- and B-group medial rectus motoneurons that supply singly innervated fibers was observed. Ultrastructural analysis demonstrated a direct synaptic linkage between anterogradely labeled reticular terminals and retrogradely labeled medial rectus motoneurons in all three groups. These findings reinforce the notion that the cMRF is a critical hub for oculomotility by proving that it contains premotor neurons supplying horizontal extraocular muscle motoneurons. The differences between the cMRF input patterns for C-group versus A- and B-group motoneurons suggest the C-group motoneurons serve a different oculomotor role than the others. The similar patterns of cMRF input to C-group motoneurons and preganglionic Edinger-Westphal motoneurons suggest that medial rectus C-group motoneurons may play a role in accommodation-related vergence.

Functional diversity of motoneurons in the oculomotor system

“…It should be noted, however, that we found significant physiological differences that could be in accordance with previous morphological studies (20)(21)(22)(23). The analysis of discharge characteristics revealed noticeably lower firing rates in MIF motoneurons compared with SIF motoneurons.…”

“…Similar conclusions have been proposed after anterograde labeling from several premotor areas to SIF and MIF oculomotor motoneurons in monkeys (20). More recent studies have also found differences in afferents to the two motoneuronal types (22,23). Our data, however, are not in accordance with the division of motoneurons into "slow" versus "fast" or "tonic" versus "phasic," nor in a segregation based on the type of eye movement in which they participate (15,20,21,31).…”

“…mainly to slow eye movements and fixations, but not to saccades (fast eye movements), whereas SIF motoneurons would participate in all types of eye movements (20)(21)(22)(23). However, oculomotor neuron activity recorded in alert animals (monkeys and cats) have shown that all motoneurons participate in all classes of eye movement (24)(25)(26)(27).…”

Neural basis of location-specific pupil luminance modulation

“…The SCi has anatomical connections to the parasympathetic and sympathetic pathways to change pupil size (11). The SCi connects to a downstream parasympathetic structure, the Edinger-Westphal (EW) nucleus, mainly via projections through the central mesencephalic reticular formation (40,41). The EW nucleus projects to the ciliary ganglion with excitatory and inhibitory connections (42) and can therefore produce constriction and dilation.…”

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

“…The characteristics of these fiber types differ considerably (see Spencer and Porter, 2006 for review) and there are also differences in the motor neurons that innervate the two fiber types. In primates, SIF motoneurons are large cells found within the extraocular motor nuclei, while MIF motoneurons are small cells found just outside the nuclear borders (Wasicky et al, 2004;Erichsen et al, 2014;Bohlen et al, 2017). In cat, medial rectus SIF and MIF motoneurons are both found within III, albeit in anatomically separate subgroups, and MIF motoneurons are smaller (Bohlen et al, 2016).…”