Proprioception in Extraocular Muscles of Mammals

Proprioceptive input from extraocular muscles (EOMs) is thought to play an important role for the development of normal binocular vision in mammals and man. Muscle spindles and Golgi tendon organs are proprioceptive organs in skeletal muscle. Interspecies variation is observed among mammals regarding the endowment with these proprioceptors their EOMs. In the last years, research focused on the investigation of so called "innervated myotendinous cylinders" (IMCs). IMCs are located at the myotendinous junction in EOMs. The ultrastructure of this nervous end organ was investigated in EOMs of rhesus monkey, cat, sheep, rabbit and in man. According to Ruskell`s first description IMCs consist of the terminal portion of a particular type of muscle fiber and its attached tendon. This myotendinous complex is ensheated by a capsule of fibrocytes. A single myelinated nerve fiber coming from the muscle, enters the tendon compartment of the IMC. After that, the nerve fiber turns and runs towards the IMC muscle fiber tip. This nerve fiber ramifies and nerve terminals establish contacts both with the collagen fibrils and with the muscle fiber. IMCs in rabbit EOMs are an exception since exclusively myoneural contacts are observed. Data in literature are conflicting regarding the functional importance of IMCs. Based on fine structural investigations IMCs in rhesus monkey, cat and sheep EOMs are thought to be proprioceptors. In human EOMs, fine structural investigations and labeling with a-bungarotoxin indicate that IMCs might combine both proprioceptor and effector qualities. By applying the same methodical approach it was demonstrated that IMCs in rabbit EOMs are predominantly effectors. Degeneration experiments also suggest a motor function of IMCs whereas in neuronal tracing experiments a proprioceptive function of IMCs was proposed. Since IMCs are located at the myotendinous junction they are of particular interest for strabismus surgery. To improve our knowledge about IMCs one strategy might be to gain more information about IMC nerve terminals. Nerve terminals in IMCs are always densely filled with clear vesicles. This feature might be interpreted as a storage of neurotransmitter. It is the aim of the project to investigate IMCs nerve terminals in two mammalian species by means of immunohistochemistry at the light- and electron microscopic level in order to clarify which neurotransmitter they may contain. A further goal of the project is to investigate the fine structure of putative sensory nerve endings in cat EOMs. These nerve endings were labeled in a previous study after the injection of neuronal tracers into the trigeminal ganglion of cat.

Our ability to localise the position of targets in the surrounding visual space is an essential part of the visual sense. To know the position of objects, is of practical importance in every day life in a wide range of activities, from simply reaching for an object to more complex tasks such as driving a car. For localising objects exactly, the central nervous system needs visual information from the retina as well as additional information which relates to the position of the eyes in the orbit. It is supposed that such non-visual information comes from sense organs (proprioceptors) in extraocular muscles (EOMs). Palisade endings are nervous end organs in the EOMs of mammals and man. Until now there is consensus that these EOM-specific organs are sensory, providing important information about the eye position. Encouraged by morphological findings of our research group, we hypothesised that palisade endings are effector (motor) organs. It was the goal of present research project to prove the motor properties of palisade endings. EOM preparation were immunostained and analysed by confocal laser scanning microscopy and transmission electron microscopy. In addition three dimensional reconstruction were done to demonstrate the complex morphology of palisade endings. Our findings confirmed our assumption. Palisade endings are supplied by cholinegric (motor) nerve fibres. We also could show that palisade endings are exclusively supplied by cholinergic nerves and have no sensory component. Palisade nerve terminals are cholinergic as well. Our surprising findings that palisade endings are effector organs were recently published in Investigative Ophthalmology and Visual Science (Konakci et al. 2005) and our article was rewarded with the cover image of the January issue. In a subsequent study we could assert the effector role of palisade endings in a primate species (Konakci et al., manuscript submitted). In contrast to the current opinion that palisade endings are sensory organs, our findings show that palisade endings fulfil an effector function. Therefore palisade endings are no candidates to provide information about the eye position. Our findings are not only of scientific interest but also have clinical relevance. Palisade endings are present in EOMs of humans and are of crucial interest for strabismus surgery.