Macaque monkey trigeminal blink reflex circuits targeting orbicularis oculi motoneurons

Abstract

The trigeminal blink reflex plays an important role in protecting the corneal surface from damage and preserving visual function in an unpredictable environment. The closing phase of the human reflex, produced by activation of the orbicularis oculi (ObOc) muscles, consists of an initial, small, ipsilateral R 1 component, followed by a larger, bilateral R 2 component. We investigated the circuitry that underlies this reflex in macaque (Macaca fascicularis and Macaca mulatta) monkeys by the use of single and dual tracer methods. Injection of retrograde tracer into the facial nucleus labeled neurons in the principal trigeminal nucleus, and in the spinal nucleus pars oralis and interpolaris, bilaterally, and in pars caudalis, ipsilaterally. Injection of anterograde tracer into the principal trigeminal nucleus labeled axons that directly terminated on ObOc motoneurons, with an ipsilateral predominance. Injection of anterograde tracer into pars caudalis of the spinal trigeminal nucleus labeled axons that directly terminated on ipsilateral ObOc motoneurons. The observed pattern of labeling indicates that the reticular formation ventromedial to the principal and spinal nuclei also contributes extensive bilateral input to ObOc motoneurons. Thus, much of the trigeminal sensory complex is in a position to supply a monosynaptic drive for lid closure, and the adjacent reticular formation can supply a disynaptic drive. These findings indicate that the assignment of the R 1 and R 2 components of the blink reflex to different parts of the trigeminal sensory complex cannot be exclusively based on subdivision connectional relationships with facial motoneurons. The characteristics of the R 2 component may be due, instead, to other circuit properties.

Macaque monkey trigeminal blink reflex circuits targeting levator palpebrae superioris motoneurons

“…So we do not believe that reticular projections are responsible for the labeled terminals observed in CC. This is a noteworthy finding, as the paratrigeminal reticular formation in the pons (Figure 14) has been implicated in activating both orbicularis oculi motoneurons and retractor bulbi motoneurons during trigeminally elicited blinks (cat: Holstege et al, 1986; Holstege & Tan, 1988; rabbit: van Ham & Yeo, 1996; macaque: May & Warren, 2021). It appears that the pontine portion of this paratrigeminal region is solely responsible for the excitatory components of the blink closing phase, and that the inhibitory circuits supplying III are instead located in the region lining the rostral edge of pV.…”

“…This downward motion is produced by relaxing the levators, which releases the tension in the check ligaments of the eyelids, pulling them downward (Evinger et al, 1991; Sibony et al, 1991). We previously showed that cells within pV and in the adjacent paratrigeminal reticular formation in the macaque do, in fact, provide a monosynaptic input to orbicularis oculi motoneurons in the contralateral facial nucleus (Figure 14, light and dark blue circuits, respectively) (May & Warren, 2021). So both the excitatory and inhibitory paths are bilateral and direct.…”

“…The inhibitory trigemino‐oculomotor pathway to the levator motoneurons located in the caudal central subdivision (CC) is shown in red. The monosynaptic excitatory pathways to the orbicularis oculi motoneurons in the facial nucleus (VII) are shown in light blue and the disynaptic excitatory pathways by way of the paratrigeminal reticular formation (PTR) are shown in dark blue (data from May & Warren, 2021). A putative excitatory pathway from the caudal portion of PTR to the oculomotor nucleus (III), which would cause retraction of the globe during a blink, is shown in brown [Color figure can be viewed at wileyonlinelibrary.com]…”

“…We did observe retrogradely labeled neurons in the caudal pontine and rostral medullary reticular formation, but not in the spinal trigeminal nucleus (Figure 11). Consequently, we examined cases in our collection with BDA injections involving the reticular formation of the caudal brainstem (May & Warren, 2021). A portion of those which produced terminal fields in the facial nucleus also displayed labeled axonal arbors in III (not illustrated).…”

A Novel Tectal/Pretectal Population of Premotor Lens Accommodation Neurons

“… 27 The sections from the WGA-HRP injection were reacted using tetramethylbenzidine with ammonium molybdate as a chromagen in 0.1 M, pH 6.0 PB, as previously described. 28 These sections were counterstained with cresyl violet. All sections were dehydrated in a graded series of ethanols, cleared in toluene, and coverslipped.…”