In Part 1 we reviewed evidence for the importance of proprioception in eye muscle function.
The graphic above is from a paper on sensory control of extraocular muscles, postulating proprioceptive pathways based on known connections. if proprioceptive signals are generated in the palisade endings on multiply innervated extraocular muscle fibers (MIFs), the information may first relay in the spinal trigeminal nucleus (Sp trig. n). From here axons project to the superior colliculus tier, which is closely interconnected to the central mesencephalic reticular formation (cMRF), and the supraoculomotor area (SOA). The cMRF and SOA are direct premotor structures for the oculomotor neurons of the MIFs.
The significance of extraocular muscle proprioception on oculomotor control was laid out beautifully by Weir, Knox, and Dutton in a review in the British Journal of Ophthalmology. Here is their conclusion:
“Knowledge of the position of the eyes within the orbits is a prerequisite for coordinated eye movements, gaze shifts, and accurate visuomotor behaviour. Although vision itself, combined with central monitoring of outflowing neural discharge to the EOM, provides much of the required information, there is now considerable experimental and clinical evidence that inflowing proprioceptive signals from the EOM make a vital contribution. Animal and human
studies have demonstrated that removing or manipulating EOM afferent input not only affects static eye position but can also modify smooth pursuit, saccades and the vestibulo-ocular reflex. A greater understanding of the role of proprioception in oculomotor control would be beneficial not only from a theoretical viewpoint but also in everyday clinical practice as strabismus surgery, a commonly performed procedure, involves manipulating areas of the extraocular muscles richly endowed with proprioceptors.
Too little attention has been paid to the visual, oculomotor, and visuomotor sequelae of muscle surgery. Thus, little is known as to what effect, if any, different methods of handling these tissues might have on surgical success. Further studies are clearly required.”
Our colleague, Dr. W.C. Maples, alludes to the need for proprioceptive therapy through “slappin’ the sockets“. Dr. David Cook addresses this in the context of ocular calisthenics, which he defines as techniques that employ vigorous monocular eye movements to extend a muscle or muscle’s range of motion. In working with young children, we typically emphasize calisthenics by following a target of interest in the direction opposite to which the eye is drifting. For infants we can use the Doll’s Eye phenomenon by rotating the head in the direction opposite to the path we want the eye to follow. Sector or binasal occlusion can be very useful in conjunction with proprioceptive therapy.
A good friend who reads the blog regularly sent along an article that reinforces this concept. It’s abstract concludes: “Binocular coordination is achieved by a neural network at the motor periphery comprised of motoneurons and specialized interneurons located near or in the cranial nerve nuclei that innervate the extraocular muscles. It is assumed that this network must be trained and calibrated during infancy and probably throughout life in order to maintain the precise binocular coordination characteristic of primate eye movements despite growth, aging effects, and injuries to the eye movement neuromuscular system. Malfunction of this network or its ability to adaptively learn may be a contributing cause of strabismus.”
There are several take-home messages here:
1) Ocular calisthenics recalibrate the stretch reflexes within neuromuscular pathways. This supports the utility of monocular therapy in strabismus, particularly when using peripheral targets such as inserting pegs into holes, or pointer in straw while the eye is in the desired position.
2) Proprioceptive feedback is aided by adding cues that help match eye position with location in space, such as lenses, prisms, auditory (sound) or kinesthetic (touch). This photo from our colleague, Dr. Fortenbacher, shows a procedure being done on the midline, whereas other procedures may be done more peripherally.
3) Motor activities are crucial scaffolding. The patient can progress from activities lying on his back, to sitting in a chair, to standing, to standing on a balance board.
The bottom line is that recalibrating proprioception monocularly to match what the patient can do with the right eye compared to the left eye is as important as ever in attaining accurate spatial localization to support binocularity.
4) A recent paper in JBO from Dr. Dasinger at SCO notes that occlusion therapy is the most common nonsurgical treatment prescribed by ophthalmologists for strabismus, whether or not amblyopia is present. Protocols vary from one hour of patching per day to full-time occlusion. Some practitioners alternate which eye is occluded, while others choose to patch the dominant eye only. Consider what may happen with this approach:
a) possibly counteracts the development of anomalous correspondence and/or suppression.
b) breaks down any binocular reflexes so that the maximum motor angle of strabismus is exhibited.
c) provides opportunities for proprioceptive recalibration.
All well and good, until one re-reads the caution above:
A greater understanding of the role of proprioception in oculomotor control would be beneficial not only from a theoretical viewpoint but also in everyday clinical practice as strabismus surgery, a commonly performed procedure, involves manipulating areas of the extraocular muscles richly endowed with proprioceptors. Too little attention has been paid to the visual, oculomotor, and visuomotor sequelae of muscle surgery. Thus, little is known as to what effect, if any, different methods of handling these tissues might have on surgical success. Further studies are clearly required.