Testing the Outflow Theory of Eye Position Sense and Finding It Wanting

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My first sabbatical was spent at the Smith Kettlewell Institute of Visual Sciences in San Francisco where the legendary strabismologist Dr. Arthur Jampol-sky taught me about strabismus and its treatment by surgery. While observing Dr. Jampolsky operate, it occurred to me that the surgically treated patient was an ideal "preparation" for studying the outflow theory of eye position. Without afferent feedback, the surgical rotation of the eye by the surgeon should not be known to the patient's central nervous system until after a period of post-operative visual feedback and adaptation.

The surprising result was that some patients we tested after surgery clearly had information that the eye had been rotated to a new position in the orbit. We assessed this by an open-loop pointing task (Steinbach and Smith, 1981). But another group of patients didn't seem to have this information, and, by examining their histories, the difference became apparent: newly operated patients had eye muscle afference while patients who were having the same muscles operated on for a second or third time did not have this information. We speculated about tendon organs at the site of much of the surgeries being the source of the information, but it wasn't until Frances Richmond was drawn into collaboration that we were able to identify the presence of palisade endings, presumed proprioceptors, at the musculotendinous junction (Richmond et al., 1984).

Further studies gave us even more reason to believe that the palisade ending is playing a role in supplying eye position information. We compared two forms of muscle-weakening procedures done to correct strabismus, the marginal myotomy and the recession (see, e.g., von Noorden, 1996, pp. 93-101). The myotomy procedure must disturb the receptors because there is crushing and cutting at the musculotendinous junction. The recession procedure involves cutting just at the insertion into the sclera, and this is some distance away from these receptors. The myotomy was more deafferenting, again measured by open-loop pointing done before and after the surgery, than was the simple recession (Steinbach, Kirshner and Arstikaitis, 1987).

Dengis et al. (1998) looked at the results of pharmacological weakening of eye muscle, achieved by injecting microgram doses of botulinum toxin (botox), on changes in registered eye position. The botox procedure, developed by Scott (1980), corrects a strabismus by allowing the antagonist muscle to draw the stra-bismic eye into a straight (orthotropic) position by weakening the muscle that keeps the eye in the incorrect position. From animal studies, it was known that the botox injection has an immediate effect on afferent responses recorded from the trigeminal nerve (Manni et al., 1989). By measuring open loop pointing responses in patients, we found that the botox had no effect in the first hour following the injection. Over days and weeks, however, there were changes that could only have resulted from a proprioceptively derived signal about eye position. We interpeted these changes as resulting from the palisades, and not from the muscle spindles also found in human eye muscles and known to be proprioceptors in other skeletal muscle (e.g., Boyd and Gladden, 1985).

These studies of visual direction shifts due to proprioceptive changes in registered eye position have all been carried out in strabismic patients. There is a large and growing literature implicating inflow sources of eye position information, in both normal subjects and in patients with other eye muscle pathologies. For example, Lewis and Zee (1993) studied a patient with an abnormal synkinesis (moving the jaw caused a movement of the eye) and showed how the registration of eye position could have only come about by the contributions to eye position of the palisade ending. Dell'Osso et al. (1999), working with a breed of dog that has congenital nystagmus, showed that cutting the recti muscles at the insertion, and then reattaching them, dampened the nystagmus. This finding has led to a clinical trial for treatment of congenital nystagmus in humans by tenotomy of the recti muscles (Hertle et al., 2001). Early results are encouraging.

The literature on the roles proprioception may play in eye movement control is burgeoning. The reader is referred to Donaldson (2000), for an excellent, comprehensive, and up-to-date review.

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