Proprioception from extraocular muscles (EOMs) provides the brain with eye position signals. Surprisingly, classical proprioceptors (muscle spindles and Golgi tendon organs) are absent in the EOMs of most mammals. Instead, palisade endings (PEs) are found as unique to EOMs of mammals. They are regularly present in frontal-eyed but infrequent in lateral-eyed species. PEs are formed by axons which extend onto the tendon where axons make a u-turn and divide into axonal branches that establish nerve terminals around the tip of a single muscle fiber. For a century, PEs have been considered as sensory structures substituting classical proprioceptors in EOMs. The interest in PEs has newly aroused when molecular analysis and recent neuronal tracing experiments have shown that PEs are cholinergic and originate from the EOM motor nuclei. Since the development of PEs is unknown, we have analyzed their postnatal maturation in a frontal-eyed species (cat). Cats of different ages (P0, P8, P22, and adult) were used and whole mount preparation of the rectus EOMs were triple-immunolabelled and analyzed in the CLMS. Triple labelling included antibody against neurofilament (to label axons), anti-synaptopysin (to label nerve terminals), anti-growth associated protein43 (GAP43, to label developing axons), and phalloidin (to label muscle fibers). At P0, no PEs were found in the rectus muscles. However, in the medial rectus we found axons extending straight onto the tendon where they extensively sprouted to establish synaptophysin-positive contacts. At P8, premature PEs were found in the medial rectus but not in the other rectus muscles. At P22, the complexity of PEs in the medial rectus had increased noticeably and formation of PEs had started in the inferior rectus. At this stage PEs were still absent in the lateral rectus and superior rectus muscle. In the adult animal, all rectus muscles contained PEs. GAP43, a marker for developing axons was highly expressed in premature PEs. GAP43 expression decreased with age and was nearly absent in PEs of adult animals. Here we show that the development of PEs in the rectus muscles occurs in a staggered fashion and is more accelerated in the medial rectus. Recently we have shown that in frontal-eyed species many more PEs are present in the medial rectus compared with the other rectus muscles. The preponderance and the quicker maturation of PEs in the medial rectus support the notion that PEs could play a role in convergence.
|Published - 2017