The functions of the proprioceptors of the eye muscles

Abstract

This article sets out to present a fairly comprehensive review of our knowledge about the functions of the receptors that have been found in the extraocular muscles--the six muscles that move each eye of vertebrates in its orbit--of all the animals in which they have been sought, including Man. Since their discovery at the beginning of the 20th century these receptors have, at various times, been credited with important roles in the control of eye movement and the construction of extrapersonal space and have also been denied any function whatsoever. Experiments intended to study the actions of eye muscle receptors and, even more so, opinions (and indeed polemic) derived from these observations have been influenced by the changing fashions and beliefs about the more general question of how limb position and movement is detected by the brain and which signals contribute to those aspects of this that are perceived (kinaesthesis). But the conclusions drawn from studies on the eye have also influenced beliefs about the mechanisms of kinaesthesis and, arguably, this influence has been even larger than that in the converse direction. Experimental evidence accumulated over rather more than a century is set out and discussed. It supports the view that, at the beginning of the 21st century, there are excellent grounds for believing that the receptors in the extraocular muscles are indeed proprioceptors, that is to say that the signals that they send into the brain are used to provide information about the position and movement of the eye in the orbit. It seems that this information is important in the control of eye movements of at least some types, and in the determination by the brain of the direction of gaze and the relationship of the organism to its environment. In addition, signals from these receptors in the eye muscles are seen to be necessary for the development of normal mechanisms of visual analysis in the mammalian visual cortex and for both the development and maintenance of normal visuomotor behaviour. Man is among those vertebrates to whose brains eye muscle proprioceptive signals provide information apparently used in normal sensorimotor functions; these include various aspects of perception, and of the control of eye movement. It is possible that abnormalities of the eye muscle proprioceptors and their signals may play a part in the genesis of some types of human squint (strabismus); conversely studies of patients with squint in the course of their surgical or pharmacological treatment have yielded much interesting evidence about the central actions of the proprioceptive signals from the extraocular muscles. The results of experiments on the eye have played a large part in the historical controversy, now in at least its third century, about the origin of signals that inform the brain about movement of parts of the body. Some of these results, and more of the interpretations of them, now need to be critically re-examined. The re-examination in the light of recent experiments that is presented here does not ...

Eye Proprioception Used for Visual Localization Only If in Conflict with the Oculomotor Plan

“…These observations would fit with a model where proprioception, although not used for visual localization, calibrates over the long term the forward model which estimates the consequences of the oculomotor command (Steinbach, 1986). Because these two sets of experiments were performed in different species with known differences in the eye proprioceptive system (e.g., extraocular muscle spindles are absent in the monkey but present in humans; Donaldson, 2000), interspecies differences could have been responsible for the apparent contradiction between their conclusions. Another possible source of discrepancy is the concern that in the experiment by Lewis et al (1998), despite the bilateral section of the trigeminal nerves, sufficient proprioceptive input could reach the CNS via the oculomotor nuclei, which have recently been suggested to receive sensory input from the pallisade endings (Lienbacher et al, 2011).…”

A stretch reflex in extraocular muscles of species purportedly lacking muscle spindles

“…Thus, our data show that our bipolar EMG recordings were sufficiently selective to exclude picking up responses of non-extraocular muscles. In addition, reflex reactions of non-extraocular muscles to eye rotations are reported to occur when the latter are combined with some other stimulation such as passive rotation of the head (Donaldson 2000), which was not the case in our experiments-our animals were anesthetized and immobilized in a stereotaxic frame. Therefore, it is also doubtful that reflex responses of neck or jaw muscles to eye rotations occurred in our animals.…”

“…Although interesting, such an experiment faces theoretical and technical challenges. Indeed, the pathway of EOM afferents has been a matter of extensive debate (for review see Donaldson 2000). When these afferent signals leave the EOM through the oculomotor nerves, they become intermixed with motor fibers (Cooper et al 1955).…”

“…It is known that stretching eye muscles evokes a sensory stimulus that could produce a synchronized response in neck or jaw muscles (Donaldson 2000;Ruskell 1999). It could be suggested that our electrodes were not sufficiently selective and picked up EMG signals from non-extraocular muscles-a "cross talk" phenomenon.…”

“…They are absent in rat EOM, sparse, absent or diminutive in EOM of non-human primates (Maier et al 1974) and present in EOM of humans (Merrillees et al 1950). Although afferent signals evoked by EOM stretching are transmitted to the central nervous system (Cooper et al 1953;Fillenz 1955;Donaldson and Long 1980;Donaldson 2000), some studies have failed to demonstrate an effect of these signals on EOM motoneurons (McCouch and Adler 1932;Keller and Robinson 1971;Carpenter 1988). This has led to the conclusion that EOM have no SRs (Keller and Robinson 1971).…”