Neural control of vergence eye movements: convergence and divergence neurons in midbrain

Animals with binocular single vision use disjunctive (vergence) eye movements to align the two eyes on a visual target. Several lines of evidence suggest that conjugate and vergence eye movement commands are generated independently and combined at the medial rectus motoneurons. If this were true, then a pure vergence eye-position signal should exist. This signal would be proportional to the horizontal angle between the eyes (vergence angle), without regard to the direction of conjugate gaze. The purpose of this experiment was to identify and study neurons that carry a pure vergence signal. Extracellular unit recordings were made from midbrain and pontine sites in monkeys trained to track visual targets moving in the horizontal, vertical, and depth (or target vergence) planes. The most commonly encountered neuron that had a vergence signal was the convergence cell. These units had a firing rate that was linearly proportional to the convergence angle; their activity was unaffected by changes in conjugate gaze. Changes in convergence cell activity preceded the change in vergence angle slightly. Convergence cell activity increased for increased convergence regardless of whether the change was in response to purely accommodative or disparity cues. Divergence cells were found far less frequently. These cells were similar to convergence cells except that they decreased their firing rate for increases in convergence. The activity of divergence cells was unaffected by changes in the direction of conjugate gaze. Both convergence and divergence cells were found, intermixed, in the mesencephalic reticular formation must outside the oculomotor nucleus. Most cells with a vergence signal were found within 1-2 mm of the nucleus. These results support the view that conjugate and vergence signals are generated independently and are combined at the extraocular motoneurons. Convergence cells seem ideally suited to provide the vergence signal required by the nearby medial rectus motoneurons.