2.2 Modeling the Binocular Alignment Control System

held in a stretched position, increased stimulation causes actual loss of sarcomeres with shortening of the basic muscle length [15, 16, 19]. This change in basic muscle length in response to the level of stimulation is precisely in the right direction to help maintain binocular alignment. In fact, it is probably the chronic average level of vergence tonus, as maintained by vergence adaptation and contributed to by the current level of fast fusional vergence, which provides the primary input to extraocular muscle length adaptation.

This further feedback mechanism, that is, vergence tonus regulating muscle length adaptation, completes the dynamic feedback system for maintenance of long-term binocular alignment (Fig. 2.1). Retinal image disparity elicits fast fusional vergence, which leads in the short term to vergence adaptation, producing a change in vergence tonus, which stimulates muscle length adaptation over a longer term, all of which reduce the retinal image disparity. Each level of this marvelous three-level feedback process also works in the direction to ease the burden on the level that precedes it. Vergence adaptation frees up fast fusional vergence to be able to respond accurately to rapid changes in retinal image disparity. Muscle length adaptation relieves vergence adaptation of excessive demands, which would otherwise saturate neuronal firing rates, and thereby e ectively resets vergence adaptation so that it can continue to function optimally in response to input from fast fusional vergence.

Basic muscle lengths

(vergence tonus)

Approx. functional muscle lengths

(acute stimulation)

Exact functional muscle lengths

[perturbation]

Retinal image disparity (diplopia)

Fast fusional vergence

Vergence adaptation

Vergence tonus

Muscle length adaptation

Fig. 2.1 T hree-level dynamic feedback system for the maintenance of binocular alignment

2.2Modeling the Binocular Alignment Control System

The basic components are now in place to model the binocular alignment control system (Fig. 2.1), beginning with the existing basic muscle length of each muscle, determined by the number of sarcomeres. Each muscle is stimulated by the current level of vergence tonus to result in the approximate functional muscle length (the physical length) to yield aligned eyes. Acute vergence stimulation supplied by fast fusional vergence completes the binocular alignment process.

However, a perturbation suddenly occurs, such as a hormonal growth spurt with a change in the divergence of the orbits, new glasses with a small change in prism e ect, or simply a switch of the object of regard from the computer screen to the bird out the window. Such a perturbation requires di erent eye alignment and will thus result in misaligned eyes for the new task if no compensation is made. Nevertheless, misaligned eyes cause retinal image disparity, with a double image of the bird out the window, which the brain does not like.

Hence, the brain responds with fast fusional vergence, changing the acute stimulation levels to the muscles. This yields new functional muscle lengths in the proper direction to compensate for the original perturbation, and realigns the eyes.

Something else now happens. Sustained fast fusional vergence leads to vergence adaptation, which adjusts the basic level of vergence tonus to ease the burden on fast fusional vergence, freeing it to be able to respond to the next perturbation.

However, there is a limit to the amount of vergence tonus that can be sustained, so something further happens. In response to the amount of overall vergence tonus, the muscle lengths slowly adapt to new basic lengths in the proper direction to reduce the original retinal image disparity. Once the basic muscle lengths have adapted, the neurologic feedback mechanisms that the original perturbation brought into play can subside, with the eyes aligned once again. Furthermore, the neurologic mechanisms can now be maximally responsive to the next perturbation.

This is the normal functioning of the long-term (as well as short-term) binocular alignment control system. This is the feedback scheme that keeps the eyes aligned during the growth of the skull in early life, throughout the development of hand–eye coordination in oblique directions of gaze, and throughout the development of presbyopia,which would otherwise cause a significant disruption of near vs. distance alignment.

2.2.1Breakdown of the Binocular Alignment Control System

However, what happens when something goes wrong

2with this feedback system? Surely it is possible that abnormalities can be present, or can develop, at various levels

within this system, any of which will lead to misalignment of the eyes. The most common abnormality is probably the absence of, or loss of, fast fusional vergence, which is simply referred to as fusion. Fusion is at a most critical position in this feedback pathway system.

If fusion does not occur in response to retinal image disparity, stimulation levels do not change appropriately, and the entire system breaks down. With loss of input from the fast fusional vergence system, the longer-term mechanisms for binocular alignment, vergence adaptation [20], and muscle length adaptation [4] become freewheeling – in other words, without guidance.

Neurologic feedback mechanisms do not necessarily shut o when their input disappears. They will often continue to function at a basal level, with a low level of output being generated. This basal output level can be biased in one direction or the other, and therefore, in this case, can continue to drive the muscle length adaptation mechanism slowly in one direction or the other, producing strabismus that was not there in the first place, or causing progressive misalignment if strabismus was already present.

A prime example of this mechanism is the phenomenon we call “sensory” exotropia. With loss of vision in one eye, fusion is lost, and as we have assumed in the past, the eye simply passively drifts outward over time. From this feedback mechanism, we can begin to understand that if one eye develops poor vision, and therefore, if the eyes have no need for convergence, the average vergence stimulation to the extraocular muscles (which had previously maintained alignment equilibrium) will shift slightly to less convergence and more divergence, actively driving the eyes into a position of exotropia. This sensory exotropia can thus be seen to be not a passive process after all, but an active driving of the eyes outward by the otherwise normal alignment mechanisms that have lost proper guidance.

2.2.2Clarification of Unanswered Questions Regarding the Long-Term Binocular Alignment Control System

The description of the above-mentioned three-stage feedback model of the long-term binocular alignment control system is not new. Upon appreciating the evidence in the

literature that muscle length adaptation can be responsive to stimulation, the above-mentioned model was first described by the author in a paper in Binocular Vision and Eye Muscle Surgery Quarterly in 1994 [4], with further elaboration in 2005 [21].The model explained how defects in fusion, or the loss of fusion, which for this purpose were considered the same as loss of vision in one eye, could lead to “sensory”-type changes in strabismus. In particular, in the torsional dimension, lack of proper feedback to the torsional control mechanism would be expected to produce what we dubbed “sensory torsion,” leading to the development of what is probably erroneously called primary oblique muscle overaction, or underaction, with accompanying A- or V-pattern strabismus.

It was not clear in 1994, however, whether extraocular muscle length adaptation responds to version stimulation. That is, will an extraocular muscle adapt its length for optimal function in the position in which it is held most of the time by version stimulation? If so, what are the relative roles of version and vergence stimulation in the regulation of extraocular muscle length? New observations have clarified these questions. These observations, the resulting clarification, and the consequences to our understanding of strabismus are expected benefits from this chapter.

2.2.3Changes in Strabismus

as a Bilateral Phenomenon

The primary new observation of the author is that changes in strabismus occur, to a large extent, bilaterally. This is not speaking of strabismus in terms of the fixation pattern, but rather in terms of the relative basic lengths of the extraocular muscles and the tonus of their innervation.

In the case of sensory exotropia, one eye is always fixing, and the other eye gradually turns outward over time. However, there is usually mild limitation of adduction of both eyes, and when that patient is put to sleep, very often both the eyes turn out. Figures 2.2–2.4 show examples of this bilateral phenomenon in patients with sensory exotropia.

This observation was first made by the author 25 years ago after a recess-resect procedure on a patient with sensory exotropia. The sensory exotropia recurred. When the patient was put back to sleep for a repeat recess-resect procedure on the same eye, the previously operated eye was straight. It was the sound eye that was turning out significantly. The muscle changes that caused the original sensory exotropia had occurred bilaterally. Arthur Jampolsky [22] reported this phenomenon in 1986, but he o ered no explanation for it.

Fig. 2.2 Eighty-year-old woman with dense amblyopia in her left eye since childhood, fixing with her right eye only, all her life. Note the left sensory exotropia (top). Under general anesthesia (bottom), both eyes turn out, equally – and significantly farther than the usual divergence seen under anesthesia

There is more evidence that changes in strabismus occur bilaterally over time. Infants with esotropia and amblyopia, where the amblyopic eye is practically constantly adducted during waking hours, usually show some limited abduction bilaterally and symmetric positions of the eyes under anesthesia. Furthermore, during surgery, both medial rectus muscles are usually equally and abnormally tight. They are both abnormally short. These children sometimes show a small head turn, fixing with the sound eye in slight adduction [23], consistent with a short medial rectus muscle in the sound eye as well as in the amblyopic eye. Figure 2.5 shows the same phenomenon in an adult with esotropia and long-standing unilateral fixation.

There is still further evidence that changes in strabismus occur bilaterally. The torsional changes that are associated with primary A and V patterns are practically always bilateral, although sometimes asymmetric. If the eye with greater elevation in adduction is operated upon with an inferior oblique weakening procedure, the other eye soon shows as much or more elevation in adduction.

Fig. 2.3 Twenty-one-year-old man with left sensory exotropia (top), from a left macular scar since birth, with counting fingers vision in his left eye. His eyes also turn out essentially equally under anesthesia (bottom)

2.2.4Changes in Basic Muscle Length

These changes in strabismus occur because the muscles change their basic length, i.e., the number of sarcomeres. A basically short muscle has fewer sarcomeres than normal, and a basically long muscle has more sarcomeres than normal. As noted before, skeletal muscles are continually changing their basic lengths throughout life, by the serial addition or subtraction of sarcomeres, for optimal function in the position where they are usually held.

However, if this were the only mechanism by which extraocular muscle basic lengths are regulated, we should expect the patient with sensory exotropia to show only the poor vision eye turning out under anesthesia, because the exodeviated eye would have adapted its muscle lengths for optimal function centered in far abduction. But this is not what we observe. Usually, both eyes in sensory exotropia turn out under general anesthesia, significantly more than the usual divergence seen under anesthesia. There must be another mechanism that causes basic muscle

Fig. 2.4 T hirty-eight-year-old man after a right optic nerve injury 15 years before, with resulting blindness in his right eye. The fixing left eye (top) turns out abnormally under anesthesia (bottom), but not as much as the blind right eye. Not every patient turns out equally

lengths to change bilaterally, and that mechanism is most surely related to stimulation, given the fact that chronic electrical stimulation has been shown to shorten muscles by causing the loss of sarcomeres [15].

2.2.5Version Stimulation

and Vergence Stimulation

What type of stimulation do the extraocular muscles normally receive? If one thinks about it, the extraocular muscles between the two eyes are yoked as much as, or more than, any other muscles in the body. They are heavily bilaterally innervated. They are linked in versions, movements of the two eyes in the same directions, and in vergences, movements of the two eyes in opposite directions. Versions allow us to look in di erent directions, while vergences allow us to change our gaze from distance to near. However, vergences also, and most importantly, fine-tune both eyes to be aligned with the object of regard, in any direction of gaze and at any distance, as part of the process of sensorimotor fusion. Disparity between the two eyes’ images invokes a fusional vergence

Fig. 2.5 T hirty-four-year-old woman with esotropia since childhood with fixation with her left eye only (top), for many years. Both eyes turn in significantly under anesthesia (bottom)

response which moves the eyes in opposite directions to eliminate image disparity, accurate to within a few minutes of arc, both horizontally and vertically.

Might one of these types of stimulation, version stimulation or vergence stimulation, be involved in the regulation of basic muscle lengths for long-term alignment of the two eyes? Clearly, version stimulation would not be expected to be useful in such regulation, because version stimulation moves both the eyes in the same direction. If the extraocular muscles do change their basic lengths in response to version stimulation, then in the normal state, the e ect would average to zero over time as the eyes look about in various directions.

Vergence stimulation, on the other hand, is precisely the type of bilateral stimulation which could play a role in muscle length adaptation. If the basic muscle lengths of the extraocular muscles are altered for any reason from their current lengths, image disparity will be sensed by the brain, and fusional vergence will occur to restore binocular alignment.The same fusional vergence that realigns the eyes momentarily, leads via vergence adaptation to changes in vergence tonus. Changes in vergence tonus, representing chronic changes in the levels of stimulation,