The design of the eye and the muscles and bone that surround it help the brain manage certain complex aspects of eye movement, according to researchers at Washington University School of Medicine in St. Louis. The finding, published in Neuron, may help push an old debate about how eye movement is controlled toward resolution and help eye surgeons better diagnose and treat disorders such as strabismus (crossed eyes) that lead to misalignment of the eyes.
The task of orienting the eyes is more complicated than it might seem at first glance, notes senior investigator Dora Angelaki, Ph.D., Alumni Endowed Professor of Neurobiology.
“When we roll our head sideways, our eyes must counter-roll or move in the opposite direction to keep the visual world stable on the retina,” Angelaki explains. “This is a well-studied reflex called the vestibulo-ocular reflex or VOR, and it’s what lets us see clearly when we walk, drive a car or turn around to see a friend.”
Adding to the complexity, rotation of a round, three-dimensional object such as the eye has a property known as non-commutativity. This means that the result of a series of motions — a quarter-turn left and a half-turn up, for example — is dependent on the order in which those motions are performed. Reverse the order of two steps in the series of motions, and the end result is different.
Scientists began to debate in the late 1980s whether the complexities of these problems were handled solely by signals from the brain or accomplished via contributions both from the brain and from the eye. The latter group theorized that the “motor plant” of the eye — which includes the eye, the orbit or eye socket and the muscles that pull on it — could handle some aspects of these tasks without input from the brain. The different models suggested very different things about the way the brain controls eye movement.
Angelaki and first author Fatema F. Ghasia, a Washington University postdoctoral fellow, conducted two sets of tests in primates. In the first, the primates tracked a moving target by moving only their eyes; in the second, the bodies or heads of the primates were rotated while their eyes remained fixed on the target, invoking VOR. In both tests, scientists electrically measured the activity of oculomotor neurons, the nerves that control eye muscles. They also measured the vertical, horizonal and torsional (toward the shoulders) movement of the eyes.
The oculomotor neurons changed their firing activity in the test that included head and body movement, demonstrating the brain’s involvement in control of VOR. But in the first test, oculomotor nerves did not significantly change their firing patterns as the primates tracked the target by moving their eyes, suggesting some of the guidance for the eye’s movements was coming from the eye itself and its surrounding tissues.
“It appears that the motor plant of the eye is equipped to solve the problem on its own, and then whenever you need to step in and override that process, the brain has a way to take over,” Angelaki explains. “Better understanding of how this ability is naturally engineered into the motor plant of the eye is going to be very important for clinical applications, because every time a surgeon manipulates the muscles around the eye it might interfere with these abilities.”
Ghasia FF, Angelaki DE. Do motoneurons encode the noncommutativity of ocular rotations? Neuron, July 21, 2005, 281-293.
Funding from the National Institutes of Health supported this research.
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