Palisade Endings Are a Constant Feature in the Extraocular Muscles of Frontal-Eyed, But Not Lateral-Eyed, Animals

Abstract

Purpose To test whether palisade endings are a general feature of mammalian extraocular muscles (EOMs). Methods Thirteen species, some frontal-eyed (human, monkey, cat, and ferret), and others lateral-eyed (pig, sheep, calf, horse, rabbit, rat, mouse, gerbil, and guinea pig) were analyzed. Palisade endings were labeled by using different combinations of immunofluorescence techniques. Three-dimensional reconstructions of immunolabeled palisade endings were done. Results In all frontal-eyed species, palisade endings were a consistent feature in the rectus EOMs. Their total number was high and they exhibited an EOM-specific distribution. In particular, the number of palisade endings in the medial recti was significantly higher than in the other rectus muscles. In the lateral-eyed animals, palisade endings were infrequent and, when present, their total number was rather low. They were only found in ungulates (sheep, calf, pig, and horse) and in rabbit. In rodents (rat, guinea pig, mouse, and gerbil) palisade endings were found infrequently (e.g., rat) or were completely absent. Palisade endings in frontal-eyed species and in some lateral-eyed species (pig, sheep, calf, and horse) had a uniform morphology. They generally lacked α-bungarotoxin staining, with a few exceptions in primates. Palisade endings in other lateral-eyed species (rabbit and rat) exhibited a simplified morphology and bound α-bungarotoxin. Conclusions Palisade endings are not a universal feature of mammalian EOMs. So, if they are proprioceptors, not all species require them. Because in frontal-eyed species, the medial rectus muscle has the highest number of palisade endings, they likely play a special role in convergence.

Palisade Endings of Extraocular Muscles Develop Postnatally Following Different Time Courses

“…Concordant with recent quantitative analyses, 10 the highest number of palisade endings was counted in the medial rectus and the lowest in the lateral rectus, whereas values for the inferior and superior rectus lay in between. Additionally, the final density of palisade endings was reached at P45 in the medial and inferior rectus, at P95 in the lateral rectus and not as early as P95 in the superior rectus.…”

“…The preponderance, early final density as well as accelerated development of palisade endings in the medial rectus strengthens our previous hypothesis that palisade endings play an important role in convergence. 10 Additional support comes from findings that the cell bodies supplying palisade endings of the medial and inferior rectus lie in a distinct group of neurons (C-group) close to the EdingerWestphal nucleus. Dendrites of the C-group neurons extend into the Edinger-Westphal nucleus increasing their synaptic density there, indicating that they might share synaptic input with preganglionic neurons related to pupil constriction and lens accommodation during convergence.…”

“…20 These findings strongly suggest that palisade endings arise from MIF motoneurons in the EOM motor nuclei although receptors for cholinergic transmission have not been found in palisade endings so far with the exception of rabbit and rat. 10,20 Following tracer injection into the distal myotendinous junction (the region of the palisade endings), two populations of neurons have been retrogradely labeled at the periphery of the oculomotor nucleus, i.e., multipolar motor-like neurons and spindle shaped sensory-like neurons. 32 It has been suggested that the latter group are the source of palisade endings.…”

“…[7][8][9] Palisade endings are regularly present in the EOMs of frontal-eyed species (human, monkey, cat, dog, and ferret) but infrequent in lateral-eyed species (i.e., they are present in ungulates [pig, cow, horse, and sheep] and rabbit), but absent in most rodents. [10][11][12] Palisade endings are located at the myotendinous junction and formed by nerve fibers that come in from the muscle and extend into the tendon. There, axons make a u-shaped turn, branch, and establish terminal varicosities at the tendon level and around single muscle fiber tips.…”

Distribution of Palisade Endings Across Species Suggests They Function in Vergence Eye Movement Control

“…In trying to understand the function of these and other eye muscle proprioceptors (see Leigh and Zee 1 for a recent summary), one must also account for their idiosyncratic presence and distribution across species. In this issue, Blumer et al 2 have produced the first systematic study of PE distribution across 13 mammalian species, both lateral-and frontal-eyed. Using immunofluorescence histological techniques, they provide beautiful images that illustrate the presence, morphology, and distribution of PEs in different rectus EOMs in the species studied.…”