Core Messages

■Patients with long-standing unilateral strabismus, such as “sensory” exotropia in the absence of fusion or esotropia with unilateral amblyopia, typically show bilateral deviations under anesthesia, often symmetric.

■Forced ductions usually show symmetric muscle tightness. Changes in extraocular muscle lengths thus appear to occur primarily bilaterally,whether or not fusion is present.

■With skeletal muscles responding to changes in stimulation by the gain or loss of sarcomeres, it is likely that abnormal or unguided vergence tonus,

which changes the lengths of the extraocular muscles bilaterally, is largely responsible for changes in the angle of strabismus over time.

■This mechanism helps explain the development of

(1)increasing “basic” deviations in accommodative esotropia, (2) torsional deviations with apparent oblique muscle “overaction/underaction” and A and V patterns, (3) recurrent esotropia with early presbyopia, (4) occasional divergence insufficiency in presbyopes, and (5) basic cyclovertical deviations that mimic superior oblique muscle paresis.

2.1Binocular Alignment System

A vexing problem in the field of strabismus is what causes strabismus to change over time. For example, why do patients with accommodative esotropia develop a basic component over time [2, 3]? Why do torsional deviations develop, with accompanying A and V patterns [4]? Why does superior oblique paresis change in its pattern of deviation over time? When vision is lost in one eye, or simply when fusion is lost, why does sensory exotropia develop? If we can get a handle on the underlying mechanism involved in these changes, we may be able to better guide our research and improve the care we give to our patients. This chapter is intended to provide some further insight to this predominant underlying mechanism that induces changes in strabismus, to a large extent, bilaterally. This does not refer to 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 vergence innervation. Before discussing the bilateral nature of strabismus changes, the two basic mechanisms are reviewed that regulate long-term binocular alignment.

2.1.1Long-Term Maintenance of Binocular Alignment

In the normal situation, sensorimotor fusion maintains binocular alignment on a moment-by-moment basis, but there are two further mechanisms that maintain binocular alignment in the long term. The first is a neurologic one, “vergence adaptation,” and the second is a muscular one,“muscle length adaptation.”

2.1.2 Vergence Adaptation

Neurologically, retinal image disparity invokes a fusional vergence response which moves the eyes in opposite

2directions to eliminate the retinal image disparity, accurate to within a few minutes of arc, both horizontally and vertically. This is sometimes called “fast” fusional vergence. It responds to retinal image disparity in less than a second, and if one eye is suddenly covered, it decays in 10–15 s or less [5].

It is feedback from fast fusional vergence that stimulates changes in tonic vergence, or vergence tonus, over time [6]. This process is sometimes called “slow” vergence, or vergence adaptation. Vergence adaptation occurs selectively for di erent directions of gaze and for di erent distances, as if the brain establishes a table of how much innervational tonus to provide to each extraocular muscle to keep the eyes aligned in each direction of gaze and at each distance – horizontally, vertically, and torsionally [7]. The e ects of vergence adaptation can persist for minutes to hours and perhaps much longer. Vergence adaptation wears o slowly when one eye is occluded or during sleep, but much faster in the presence of a competing vergence [6]. This mechanism was phenomenologically described as long ago as 1868 by Hering (cited in [8]), and in 1893 by Maddox (cited in [9]). Alfred Bielschowsky actually studied this early in his career, reporting with Hofmann in 1900 that vergence adaptation decays slowly, and with an exponential time course (cited in [10]). It has been studied extensively by Ellerbrock [8], Ogle and Prangen [11], Carter [6], Crone [12], Schor [10], and many others [9]. Clearly, by supplying learned tonus levels to keep the eyes roughly aligned in various direction of gaze, vergence adaptation significantly eases the burden on sensorimotor fusion, leaving sensorimotor fusion free to fine-tune the alignment of the eyes [6].

Vergence adaptation provides a tonic neural compensation for ocular deviations. It eliminates the anisophoria produced by new anisometropic spectacle lenses. It begins to decay slowly when one eye is covered, as evidenced by the “screening-up” of ocular deviations when measuring with the prism and alternate cover test. In the longer term, it is responsible for the “eating up” of prisms over minutes to days in the process called prism adaptation. Clinically, we often try to uncover the underlying deviation by occluding one eye. For example, Lancaster redgreen plots of incomitant strabismus with partial fusion often show best alignment in primary gaze, and in the reading position, those directions of gaze that are most used and, therefore, best adapted to. After a 30-min patch test, the plotted tropia often increases in these directions

of gaze, with increased comitance of the overall pattern of deviation [13].

However, maximum neuronal firing rates impose limits on how much misalignment can be compensated for by vergence adaptation. In particular, orbital changes with skeletal growth require not only lengthening of the extraocular muscles, but also require relative changes in functional muscle length that are far beyond the capabilities of neurologic adaptation. It is the process of muscle length adaptation that comes to the rescue.

2.1.3Muscle Length Adaptation

The topic of muscle length adaptation does not appear in most texts on strabismus. The historic assumptions have been that extraocular muscle lengths are determined genetically, and that the basic forms of strabismus are due to primary abnormalities in muscle anatomy, in innervation, or in neurologic tonus. However, there must be dynamic mechanisms involved in the regulation of basic muscle length which normally play a critical role in the long-term maintenance of binocular alignment.

Tracer studies have shown that skeletal muscles throughout the body undergo continuous remodeling throughout life. In fact, the half-life of the contractile proteins in adult skeletal muscles is only 7–15 days [14]. Muscle physiologists in France and England [14– 16] discovered in the 1970s and 1980s that skeletal muscles intrinsically adapt their lengths, by serial addition or subtraction of sarcomeres at the ends of the myofibrils, to maintain the proper overlap of the actin and myosin myofilaments so as to obtain optimal force generation, velocity, and power output over the range of motion through which the muscle is most used [17]. The exact biologic mechanism that accomplishes this is still unknown.

In 1994, Alan Scott [18] showed that the extraocular muscles can adapt their lengths in the same way as the other skeletal muscles throughout the body. He sutured one eye of a monkey to the lateral orbital wall in an exotropic position of approximately 30 prism diopters. After 2 months, when the basic lengths of the extraocular muscles were examined, the medial rectus muscle had gained sarcomeres, and the lateral rectus muscle had lost sarcomeres in the experimental animal, compared with control animals operated in the same manner and sacrificed immediately.

Change in skeletal muscle length is not only responsive to the position in which the muscle is held, but also, and most importantly, in the case of the extraocular muscles, to the stimulation that it receives. If a muscle is not