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Sherrington's Law of Reciprocal Innervation

AGONIST, ANTAGONIST, AND YOKE MUSCLES. As a rule, every contraction of a muscle brings
about a movement. Considered as the mover producing that movement, the muscle is called an
agonist. A movement in the direction opposite that produced by the agonist is caused by its
antagonist. Thus, the medial rectus muscle adducts the globe, and the lateral rectus muscle abducts
it. The medial and lateral rectus muscles are antagonists.
Two muscles moving an eye in the same direction are synergists. The superior oblique muscle and
the inferior rectus muscle are both depressors of the eye. As such they are synergists. However, the
superior oblique muscle causes an incyclorotation and the inferior rectus muscle, an excyclorotation.
In respect to cyclorotation, they are antagonists.
Synergistic muscles in the two eyesmuscles that cause the two eyes to move in the same direction
are known as yoke muscles. Some readers may not be familiar with the word yoke. In fact, in
correcting examination papers and even in the ophthalmic literature we have seen this word not
infrequently misspelled yolk. The reader who grew up in an urban society or in a country where draft
animals have been replaced by agricultural machines may not know that yoke refers to a wooden
bar or frame by which two draft animals (e.g., oxen) are joined at the head or necks for working
together.133 When one yoked animal moves in a certain direction, so must the other, and the same
applies to the cooperation between a pair of yoke muscles. In passing we note that although there are
words for yoke in many languages, this vivid and didactically useful allegory in explaining the
functional linkage between the extraocular muscles of the two eyes is to our knowledge limited to the
English ophthalmic literature (see also Chapter 20).
The right medial rectus and the left lateral rectus muscles cause levoversion of the eyes. They are
yoke muscles. As pointed out earlier in this chapter, a pair of muscles in one eye can be yoked with a
pair in the other eye. For instance, the elevators of one eye (superior rectus and inferior oblique
muscles) are yoked as a unit to the elevators of the fellow eye, and the two pairs of depressors are
similarly yoked. Thus, antagonistic muscles act on the same eye, and yoke muscles act on both eyes.
Yoking may change according to the different type of eye movements. For instance, the medial rectus
muscle of one eye is yoked with the lateral rectus muscle of the other eye in lateroversion, but the
medial rectus muscles in both eyes are yoked during convergence.
The term contralateral antagonist, used in connection with so-called inhibitional palsy (see Chapter
20), is contradictory and should be avoided. This term refers to the antagonist of the yoke muscle. For
example, a patient with paralysis of the right superior oblique muscle who habitually fixates with the
right eye will have an apparent paresis of the left superior rectus muscle. The explanation for this is
that in the fixating eye the innervation of the pairs of elevators (superior rectus and inferior oblique
muscles) is below normal because of loss of the opposing action of the paralyzed superior oblique
muscle. Thus, in accordance with Herings law (see p. 64), equally diminished innervation will flow to
the elevators of the left eye and the left eye does not elevate fully. Elevation will become normal,
however, when the left eye takes up fixation.
SHERRINGTONS LAW. Whenever an agonist receives an impulse to contract, an equivalent
inhibitory impulse is sent to its antagonist, which relaxes and actually lengthens. This is Sherringtons
law of reciprocal innervation,121 which implies that the state of tension in the agonist exerts a
regulatory influence on the state of tension in the antagonist and vice versa. The finely graded
interplay between opposing eye muscles makes movements of the globe smooth and steady.

Whether there are actually active centrifugal inhibitory neural impulses flowing to the antagonist as
the agonist contracts or whether there is merely an absence of innervation is not clear. Sherringtons
law applies to all striated muscles of the body and is not limited to the extraocular muscles.
The basic mechanism underlying agonistic and antagonistic muscle action was clearly understood by
Descartes22, 30 more than 250 years before Sherringtons classic experiment 121, 122 in which he
demonstrated reciprocal innervation of the extraocular muscles. When Sherrington severed cranial
nerves III and IV intracranially on one side (e.g., on the right), a paralysis occurred in all the
extraocular muscles except the lateral rectus muscle, which was innervated by cranial nerve VI. The
right globe was now in divergent position. After allowing time for the motor nerves to the extraocular
muscles to degenerate, Sherrington electrically stimulated the right cortical area, eliciting a conjugate
deviation of the eyes to the left. The left eye turned all the way to the left, but the right eye moved only
to the midline. This behavior of the right eye gave evidence that the original divergent position was
the result of a contraction of the right lateral rectus muscle, which was unopposed by the tonus of its
antagonistic right medial rectus muscle. When a levoversion impulse was induced, the reciprocal
innervation to the right lateral rectus muscle caused it to relax to the point where the globe could
return to the midline.
The validity of Sherringtons law of reciprocal innervation now has been established in intact human
eyes by means of electromyography. Figure 410 demonstrates electrical silence in the left lateral
rectus muscle with the eyes in extreme dextroversion and in the right medial rectus in extreme
levoversion. A comparable result is achieved when recordings are made from horizontal rectus
muscles during calorically induced nystagmus.

FIGURE 410. Electromyographic evidence for reciprocal innervation of extraocular muscles. Upper tracing
from left lateral rectus muscle (LLR); lower tracing from left medial rectus muscle (LMR). In extreme right
lateral gaze (RLG) the LLR is electrically silent and the LMR is electrically active. In extreme left lateral gaze
(LLG) the LMR is electrically silent and the LLR is electrically active. (Courtesy of Dr. Goodwin M. Breinin.)

Reciprocal innervation is physiologically and clinically important. It explains why strabismus occurs
following paralysis of an extraocular muscle. Reciprocal innervation must be considered when
surgery on the extraocular muscles is performed. Co-contraction of antagonistic muscles instead of
relaxation of the antagonist, for instance, as demonstrated by electromyography in the retraction
syndrome (see Chapter 20), is said to be always abnormal in eye muscles, although it does occur in
skeletal muscles. Some clinical applications of Sherringtons law are shown in Figure 411.

FIGURE 411. Sherringtons law of reciprocal innervation. A,


On levoversion, increased contraction () of the right medial
rectus (RMR) and left lateral rectus (LLR) is accompanied by
decreased tonus (0) of the antagonistic right lateral (RLR) and
left medial rectus (LMR) muscles. B, Increased activity of both
medial rectus muscles and decreased tonus of both lateral
rectus muscles during convergence. C, Contraction and
relaxation of opposing muscle groups on dextrocycloversion
when the head is tilted to the left shoulder. RSO, right superior
oblique; RSR, right superior rectus; LSO, left superior oblique;
LSR, left superior rectus; RIO, right inferior oblique; RIR, right
inferior rectus; LLO, left inferior oblique; LIR, left inferior
rectus. (From Noorden GK von: Atlas of Strabismus, ed 4. St.
Louis, MosbyYear Book, 1983.)