Copyright © 1999 Massachusetts Institute of Technology
Eye movements fall into two broad classes. Gaze-stabilization movements shift the lines of sight of the two eyes to precisely compensate for an animal's self-motion, stabilizing the visual world on the RETINA. Gaze-aligning movements point a portion of the retina specialized for high resolution (the fovea in primates) at objects of interest in the visual world.
In mammals, gaze-stabilization movements are accomplished by two partially independent brain systems. The vestibulo-ocular system employs the inertial velocity sensors attached to the skull (the semicircular canals) to determine how quickly and in what direction the head is moving and then rotates the eyes an equal and opposite amount to keep the visual world stable on the retina. The optokinetic system extracts information from the visual signals of the retina to determine how quickly and in what direction to rotate the eyes to stabilize the visual world.
Gaze-aligning movements also fall into two broad classes: saccades and smooth pursuit movements. Saccadic eye movements rapidly shift the lines of sight of the two eyes, with regard to the head, from one place in the visual world to another at rotational velocities up to 1000°/sec. Smooth pursuit eye movements rotate the eyes at a velocity and in a direction identical to those of a moving visual target, stabilizing that moving image on the retina. In humans and other binocular animals, a third class of gaze-shifting movements, vergence movements, operates to shift the lines of sight of the two eyes with regard to each other so that both eyes can remain fixated on a visual stimulus at different distances from the head.
In humans, all eye movements are rotations accomplished by just six muscles operating in three antagonistic pairs. One pair of muscles located on either side of each eyeball controls the horizontal orientation of each eye. A second pair controls vertical orientation and a third pair controls rotations of the eye around the line of sight (torsional movements). These torsional movements are actually quite common, though usually less than 10° in amplitude.
These six muscles are controlled by three brain stem nuclei. These nuclei contain the cell bodies for all of the motor neurons that innervate the oculomotor muscles and thus serve as a final common path through which all eye movement control must be accomplished. Engineering models of the eye and its muscles indicate that motor neurons must generate two classes of muscle forces to accomplish any eye rotation: a pulsatile burst of force that regulates the velocity of an eye movement and a long-lasting increment or decrement in maintained force that, after the movement is complete, holds the eye stationary by resisting the elasticity of the muscles which would slowly draw the eye back to a straight-ahead position (Robinson 1964). Physiological experiments have demonstrated that all motor neurons participate in the generation of both of these two types of forces.
These two forces, in turn, appear to be generated by separable neural circuits. In the 1960s it was suggested that changes to the long-lasting force required after each eye rotation could be computed from the pulse, or velocity, signal by the mathematical operation of integration. In the 1980s the lesion of a discrete brain area, the nucleus prepositus hypoglossi, was shown to eliminate from the motor neurons the long-lasting force change required for leftward and rightward movements without affecting eye velocity during these movements (Cannon and Robinson 1987). This, in turn, suggested that most or all eye movements are specified as velocity commands and that brain stem circuits involving the nucleus prepositus hypoglossi compute, by integration, the long-lasting force required by a particular velocity command. More recently, a similar circuit has been identified that appears to generate the holding force required for upward, downward, and torsional movements.
The saccadic system, in order to achieve a precise gaze shift, must supply these brain stem circuits with a command that controls the amplitude and direction of a movement. Considerable research now focuses on how this signal is generated. Current evidence indicates that this command can originate in either of two brain structures: the superior colliculus of the midbrain or the frontal eye fields of the neocortex. Both of these structures contain laminar sheets of neurons that code all possible saccadic amplitudes and directions in a topographic maplike organization (Robinson 1972; Wurtz and Goldberg 1972; Bruce and Goldberg 1985). Activation of neurons at a particular location in these maps is associated with a particular saccade, and activation of neurons adjacent to that location is associated with saccades having adjacent coordinates. Lesion experiments indicate that either of these structures can be removed without permanently preventing the generation of saccades. How these signals that topographically encode the amplitude and direction of a saccade are translated into a form appropriate for the control of the oculomotor brain stem is not known. One group of theories proposes that these signals govern a brain stem feedback loop which accelerates the eye to a high velocity and keeps the eye in motion until the desired eye movement is complete (cf. Robinson 1975). Other theories place this feedback loop outside the brain stem or generate saccadic commands without the explicit use of a feedback loop. In any case, it seems clear that the superior colliculus and frontal eye fields are important sources of these signals because if both of these structures are removed, no further saccades are possible (Shiller, True, and Conway 1980). The superior colliculus and frontal eye fields, in turn, receive input from many areas within the VISUAL PROCESSING STREAMS, including the VISUAL CORTEX, as well as the BASAL GANGLIA and brain structures involved in audition and somatosensation. These areas are presumed to participate in the processes that must precede the decision to make a saccade, processes like ATTENTION.
In the smooth pursuit system, signals carrying information about target MOTION are extracted by motion-processing areas in visual cortex and then passed to the dorsolateral pontine nucleus of the brain stem. There, neurons have been identified which code either the direction and velocity of pursuit eye movements, the direction and velocity of visual target motion, or both. These signals proceed to the cerebellum where neurons have been shown to specifically encode the velocity of pursuit eye movements (Suzuki and Keller 1984). These neurons, in turn, make connections with cells known to be upstream of the nucleus prepositus hypoglossi (the integrator of the oculomotor system described above). As in the saccadic system, the brain stem integrator appears to compute the long-term holding force from this signal and then to pass the sum of these signals to the motor neurons.
All eye movement control signals must pass through the ocular motor neurons which serve as a final common path. In all cases these neurons carry signals associated both with the instantaneous velocity of the eye and the holding force required at the end of the movement. Eye movement systems must provide control signals of this type, presumably by first specifying a velocity command from which changes in holding force can be computed. In the case of saccades, this command is produced by brain structures that topographically map all permissible saccades in amplitude and direction coordinates. In the case of pursuit, the brain appears to extract target motion and to use this signal as the oculomotor control input. Together these systems allow humans to redirect the lines of sight to stimuli of interest and to stabilize moving objects on the retina for maximum acuity.
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Copyright © 1999 Massachusetts Institute of Technology