Eye movement has a number of features that distinguish it from other motor behavior. In comparison with the movement that limbs, with their multiple joints and muscles, can perform, eye movement is relatively simple. For example, each eye is controlled by only three agonistantagonist muscle pairs: the medial and lateral recti, the superior and inferior recti, and the superior and inferior oblique muscles. These muscles allow the eye to rotate about three axes. Assuming that the head is in an upright position, the axes are the vertical axis, a horizontal axis that runs left to right, and the torsional axis (which is directed along the axis of sight). The medial and lateral recti control movement about the vertical axis; the other four muscles generate movement about the horizontal and torsional axes. Another simplifying feature is that there are no external loads for which to be compensated. Furthermore, eye movement appears to be separable into a few distinct types, with each type being controlled by its own specialized circuitry. Thus eye movement offers a number of advantages as a model system for studying motor control. Moreover, deficits in eye movement provide important clinical clues to the diagnosis of neurological problems. We first review the different eye movement types and then discuss the neural circuitry underlying their generation.
Types of Eye Movement
Eye movement probably first evolved to hold the image of the external world still. (In contrast, limb movements evolved to generate changes in the position of the limb with regard to the external world.) The reason is that visual acuity degrades rapidly when there is eye movement in relation to the external world (i.e., the visual scene slips across the retina). A major cause of such slippage is movement of the head. The vestibuloocular reflex (VOR) is one of the main mechanisms by which head movement is compensated in order to maintain stability of the visual scene on the retina.
To maintain a stable visual scene on the retina, the VOR produces movements of the eyes that are equal and opposite the movement of the head. This reflex is initiated by stimulation of the receptors (hair cells) in the vestibular system (see ). Recall that the vestibular organs are sensitive to head acceleration, not visual cues, and thus the VOR occurs in both the light and dark. Functionally, it is what is called an open-loop system in that it generates an output (eye movement) in response to a stimulus (head acceleration), but its immediate behavior is not regulated by feedback about the success or failure of its output. It is worth noting, however, that in the light at least, any failure by the VOR to match eye and head rotation results in what is called retinal slip (i.e., slip of the visual image across the retina), and this error signal can be fed back to the VOR circuits by other neuronal pathways and over time can lead to adjustments in the strength of the VOR to eliminate the error. This adaptation of the VOR is a major model for studying plasticity in the brain.
As stated, acceleration signals initiate the VOR. The output of the VOR, however, must be a change in eye position in the orbit. Thus the problem to be solved by the nervous system is to translate the acceleration signals sensed by the vestibular organs into correct positional signals for the eyes. Mathematically, this can be thought of as a double integration. The first integration occurs in the vestibular receptor apparatus because although the hair cells respond to head acceleration, the signals in the vestibular afferent fibers are proportional to head velocity (at least for most stimuli that are encountered physiologically). The second integration, from velocity to position, occurs in the CNS in circuits described later.
The head can move in six different ways, often referred to as six degrees of freedom: three translational and three rotational. To compensate for these different types of movement, there are both translational and angular VORs, as well as separate subsystems for handling movement about different directions (e.g., rotation about a vertical or a horizontal axis).