Eye Movements


Photoreceptors are sensitive but slow, and all animals with image-forming eyes have mechanisms to prevent images of interest from moving across the retina too quickly to be analyzed. (Our eyes behave in many respects like cameras with a shutter speed of about of a second.) A widespread strategy is to use some combination of eye movements and head or body movements to keep the direction of gaze constant, except for brief periods during which gaze shifts ( Fig. 21.1 ). Additional complications are added by having a fovea, which results in good spatial acuity for only a small area of central vision (see Fig. 17.18 ). Finally, effective binocular vision requires precise alignment of the two eyes. All this necessitates a highly accurate system for controlling eye position and movement.

Fig. 21.1
Gaze-holding by several different animal species, interrupted by quick movements that redirect gaze. (A) through (D) are seen from above as they go about various activities, (E) and (F) from the side. (A) Movements of the right eye and head of a human standing at a sink and filling a kettle, getting ready to prepare a cup of tea. Most of the time his head and eyes move in exactly opposite directions, so the direction of gaze (the sum of eye and head movement) does not change; one such period is indicated by shading. Every few hundred milliseconds his eyes move rapidly (blue arrow), shifting his gaze ( green arrow; in this case, from the right faucet-handle to the stream of water flowing into the kettle). (B) The orientation of the head, right eye, and gaze of a goldfish, as it turns while swimming in a tank of water. (C) A rock crab (Pachygrapsus marmoratus) uses the same strategy as it walks around. The head obviously cannot move independently, but the eyestalks move to counteract body/head movements; periodic faster movements of the eyestalks redirect gaze. (D) The eyes of flies are fixed in their heads and cannot move independently, but this blowfly (Calliphora erythrocephala) uses slow and fast head movements to compensate for body movements and to redirect gaze. (E) Many species of birds appear to bob their heads back and forth as they walk, but this is illusory. What they really do is take advantage of their long necks to thrust their heads forward, then hold their heads stationary until the body catches up. These successive frames from a videocamera show a pigeon (E1, E3) and a crane (E2, E4) walking from left to right. E1 and E2 are just after a head thrust has been completed, E3 and E4 are just before another one starts. During each step, the beak stays stationary, one foot (arrowhead) stays planted, and the other foot (asterisk) and the body move forward. (F) Relative positions of the body and head (and gaze) of a pigeon as it walks, showing periods of stable gaze in between head thrusts.

(A–D, modified from Land MF: J Comp Physiol A185:341, 1999. B, redrawn from Easter SS Jr, Johns PR, Heckenslively D: J Comp Physiol 92:23, 1974. C, redrawn from Paul H, Nalbach H-O, Varjú D: J Exp Biol 154:81, 1990. D, redrawn from Land MF: Nature 243:299, 1973. E, from Necker R: J Comp Physiol A193:1177, 2007. F, redrawn from Frost BJ: J Exp Biol 74:187, 1978.)

Our eyes do a fairly remarkable job of tracking (or moving to look at) various objects as we and the objects move about in three-dimensional space. Throughout this process the two eyes stay appropriately aligned with each other. Two general types of movement are involved: (1) conjugate movements, in which the two eyes move the same amount in the same direction, as when visually tracking an object moving about at a fixed distance from us, and (2) vergence movements, in which the two eyes move in opposite directions, as in the convergence that occurs when looking at a nearby object. Normally, conjugate and vergence movements are smoothly integrated, so images of the outside world fall on the two retinas in proper registration. The central nervous system (CNS) circuits that control eye movements for these various purposes have many properties in common with those described in the last three chapters for the control of other skeletal muscles—upper and lower motor neurons, central pattern generators, and interactions with the basal ganglia and cerebellum.

Six Extraocular Muscles Move the Eye in the Orbit

Six small extraocular muscles ( Fig. 21.2 ) rotate each eye in its orbit, like a ball in a socket. Four rectus (“straight”) muscles ( medial, lateral, superior, and inferior ) originate from a common tendinous ring (the annulus of Zinn) in the back of the orbit and insert anteriorly in the sclera, 5 to 8 mm from the limbus. Two oblique muscles, as the name implies, pass obliquely over the surface of the eye and insert in the sclera of its posterior half. The superior oblique originates near the common tendinous ring, from the sphenoid bone at the back of the orbit, but it takes an unusual course in reaching the eye. Near the front of the orbit, the superior oblique tendon passes through a fibrous loop (the trochlea a

a Trochlea, from which the fourth cranial nerve derives its name, is Greek for “pulley.”

) attached to the frontal bone, turns laterally and posteriorly, and inserts in the sclera of the posterior half of the eye. The inferior oblique originates anteriorly and medially from the floor of the orbit, passes across the inferior surface of the eye, and inserts posteriorly.

Fig. 21.2, Anterior (A), superior (B), and inferior (C) views of the extraocular muscles of the right eye.

Different patterns of contraction of the six extraocular muscles rotate the eye horizontally ( adduction = toward midline, abduction = away from midline), vertically ( elevation = up, depression = down), or around its anterior-posterior axis ( extorsion = rotate out, intorsion = rotate in) ( Fig. 21.3 ). As you recall from Chapter 12 , these muscles are innervated by three sets of cranial nerves. Cranial nerve III (oculomotor) innervates the majority of the muscles, including the superior, medial, and inferior rectus as well as the inferior oblique. The lateral rectus is innervated by cranial nerve VI (abducens), and the superior oblique is innervated by cranial nerve IV (trochlear).

Fig. 21.3, Terminology for eye movements around different axes.

The Medial and Lateral Recti Adduct and Abduct the Eye

The medial and lateral recti are situated in a horizontal plane, so contractions of these muscles rotate the eye around a vertical axis. This makes their actions straightforward ( Fig. 21.4 ): the medial rectus adducts and the lateral rectus abducts the eye. Both muscles pass through sleeves of connective tissue (referred to as pulleys ) as they travel from the common tendinous ring toward the eye, emerging a little posterior to their insertion points on the sclera. The pulleys, in turn, have connective tissue attachments to the walls of the orbit, so the positions of the muscles are constrained within the orbit as the eye moves. As a result, adduction and abduction continue to be the principal effects of the medial and lateral recti, even if the eye starts out in an elevated or depressed position ( Fig. 21.5 ). The superior and inferior recti and the inferior oblique have similar pulleys (in this sense, the superior oblique is not as different from the other extraocular muscles as it seems to be). The pulleys form important parts of an elaborate mechanical suspension system that helps control rotations of the eye; half the fibers of the recti and inferior oblique actually attach to the pulleys rather than the sclera, adjusting pulley positions as the eye moves.

Fig. 21.4, Actions of the medial and lateral recti of the right eye.

Fig. 21.5, Limitation of the action of the lateral rectus by its connective tissue suspension within the orbit. (A) With the eyes in primary position, the lateral rectus extends along the equator of the eye and abducts it by rotating it around a vertical axis. (B) If the lateral rectus was attached only at its origin at the common tendinous ring and its insertion in the sclera, intermediate parts of it would be free to slide over the surface of the eye during eye movements. If the eye was elevated, for example, the insertion point would move above the center of rotation of the eye, and lateral rectus contraction would elevate the eye further in addition to abducting it. (C) The functional insertion of the lateral rectus is the point at which it emerges from its connective tissue sleeve, so even if the eye is elevated, contraction mainly causes abduction.

The Superior and Inferior Recti and the Obliques Have More Complex Actions

The actions of the superior and inferior recti and the obliques are not quite so straightforward, because the anatomical axis of the orbit is deviated about 23 degrees laterally from the visual axis of the eye ( Fig. 21.6 ). The result, as indicated for the superior rectus and superior oblique in Fig. 21.7 but equally true for the inferior rectus and inferior oblique, is that when one of these muscles contracts, it looks as though the eye should rotate around an axis that is neither vertical nor transverse nor anterior-posterior. Consequently, each of these four muscles has one principal action and weaker additional actions ( Fig. 21.8 ). However, the pulley system constrains their directions of pull, and these secondary actions come into play only in eccentric gaze. Starting from straight-ahead gaze, the superior and inferior recti largely take care of elevation and depression, respectively; similarly, the superior and inferior obliques cause intorsion and extorsion, respectively.

Fig. 21.6, Relative orientations of the eyes and orbits. (A) The eye, when focused for far vision, points more or less straight ahead so that images land on the fovea (f). Because the lateral wall of each orbit is oriented about 45 degrees from the sagittal plane, the axis of the orbit, along which the superior and inferior recti appear to pull, is oriented about 23 degrees from the visual axis. (B) Computed tomography scan of a 68-year-old man showing the relationship between the eyes and the medial and lateral walls of the orbits. L, Lateral rectus; M, medial rectus; O, optic nerve.

Fig. 21.7, Apparent directions of pull and axes of rotation of the right superior rectus (A) and superior oblique (B), relative to the axes of rotation for pure torsion or pure elevation or depression. In reality, connective tissue suspensions make the superior rectus more of a pure elevator and the superior oblique more of a pure intorter than these diagrams indicate.

Fig. 21.8, Actions of the right superior and inferior recti and obliques. Each has a primary action (large arrows) and two secondary actions (small arrows) when starting from the primary position. The actions are determined by the direction of insertion of a muscle's tendon and by the position of the insertion. For example, the superior rectus and superior oblique both insert on the superior surface of the globe. However, the superior rectus inserts anteriorly and pulls posteriorly, so it elevates the eye. In contrast, the superior oblique inserts posteriorly and pulls in part anteriorly (see Fig. 21.7 ), so part of its action is depression. The extent of the secondary actions of the superior and inferior recti is somewhat exaggerated in this figure; connective tissue pulleys constrain their actions to nearly pure elevation and depression, respectively, in straight-ahead gaze.

To keep things reasonably simple in this chapter, torsional movements are not discussed, b

b We tend not to think much about torsional movements, but if you tilt your head to one side, both of your eyes counterrotate in partial compensation. Such tilting does not disturb images on the fovea too much, so torsional movements are less important for us than for more lateral-eyed animals.

and adduction, abduction, elevation, and depression are treated as the result of contraction of just one of the rectus muscles. However, eye movements actually involve coordinated changes in the activity of all six extraocular muscles ( Table 21.1 ), some contracting and some relaxing in response to changing levels of input from the oculomotor, trochlear, and abducens nuclei (see Fig. 12.4, Fig. 12.5, Fig. 12.6 ). For example, adduction involves simultaneous contraction of the medial, superior, and inferior recti and relaxation of the lateral rectus and the superior and inferior obliques; the intorsion and extorsion of the superior and inferior recti cancel each other.

TABLE 21.1
Extraocular Muscles Contributing to Movements Around Different Axes
Movement Principal Muscle Other Muscles Contributing
Adduction Medial rectus Superior rectus
Inferior rectus
Abduction Lateral rectus Superior oblique
Inferior oblique
Elevation Superior rectus Inferior oblique
Depression Inferior rectus Superior oblique
Extorsion Inferior oblique Inferior rectus
Intorsion Superior oblique Superior rectus

There Are Fast and Slow Conjugate Eye Movements

Conjugate movements serve one of two general purposes: to move an object's image onto the fovea or to keep it there (see Fig. 21.1 ). We use fast, steplike eye movements called saccades (from a French word meaning “a pull on the reins”) to redirect gaze so that a different image falls on the fovea. The same neural machinery comes into play whenever these brief, rapid movements are called for—to move our eyes voluntarily in any given direction, to glance over at something in the periphery, and in the fast phase of nystagmus. We use multiple kinds of smooth, slower eye movements to keep an image on the fovea, corresponding to the fact that an image can move on the retina if we move or if the object moves. The vestibuloocular reflex (VOR) (see Figs. 14.31 and 14.32 ) compensates for head movements, supplemented in this function by optokinetic movements (see Fig. 14.33A ); for large head movements, these smooth eye movements become the slow phase of nystagmus. Smooth pursuit movements are used to track a visual stimulus that is moving. Without special training, we are unable to move our eyes smoothly unless an image starts to leave the fovea ( Box 21.1 ).

Box 21.1
Smooth Eye Movements Usually Require Either a Vestibular Stimulus or a Target Moving Across the Retina

It generally comes as a surprise that, with the head stationary, we cannot voluntarily move our eyes smoothly unless we are tracking a slowly moving object ( Fig. 21.9A ). This is easily demonstrated, however. Watch someone's eyes as he or she tries to move them slowly and smoothly while there is nothing to track, or concentrate on your own eyes while you try to do the same thing. In either case the result will be the same: a series of rapid, jerky movements (saccades; see Fig. 21.9B ). Some individuals can learn to have voluntary control of smooth tracking movements, but under normal circumstances and for most people, this is impossible. Interestingly, real moving stimuli in other sensory modalities provide, to varying degrees, an adequate stimulus for some smooth movements. For example, many people can use smooth eye movements to track their own index fingers moving back and forth in the dark (see Fig. 21.9C ), even though they are unable to use such eye movements to track imaginary moving fingers. Similarly, smooth eye movements can be used to track a moving sound source in the dark (although less successfully than when using a somatosensory stimulus).

Fig. 21.9, Recordings of the horizontal eye movements of a normal subject in an otherwise dark room as he tracked an LED moving back and forth (A), tried to imagine an LED moving back and forth and track it with his eyes (B), and tried to follow the position of his finger as he moved his arm back and forth in the dark (C); upward deflections indicate movement to the right. Movements with a somatosensory assist are much smoother than those with only an imaginary target. You can approximate this experiment by closing your eyes and concentrating on how they move as you try to track an imaginary target or your own moving finger.

A network of neural structures distributed through the brainstem, cerebellum, and cerebral hemispheres is involved in the initiation and coordination of conjugate eye movements ( Fig. 21.10 ). Basically it involves reflex connections and central pattern generators for these eye movements, located in the brainstem, together with cerebral and cerebellar centers that are able to trigger or modulate these brainstem mechanisms. The brainstem centers differ for different kinds of movement, but the cerebral and cerebellar centers overlap. No corticobulbar fibers reach the abducens, trochlear, or oculomotor nuclei directly (see Figs. 21.13 and 21.16 ).

Fig. 21.10, Schematic overview of eye movement control systems. Central pattern generators in the brainstem project through lower motor neurons to extraocular muscles, as indicated. Interconnections between the cerebellum, basal ganglia, and cerebral centers that initiate eye movements are described further in the text; this schematic overview is not meant to indicate, for example, that the basal ganglia project directly to the central pattern generators.

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