Integration of Motion Signals for Smooth Pursuit Eye Movements

How does the brain combine local motion measurements to form an accurate description of object motion? For example, if a vertically oriented bar moves upward and rightward at a constant velocity, a neuron with a small receptive field positioned along the length of the contour can measure only the rightward component of motion, since the upward component provides no time-varying information within its receptive field. In contrast, cells positioned at the endpoints of the contour can measure motion direction accurately. Because direction-selective neurons early in the visual pathways have small receptive fields, the visual system is constantly faced with this “aperture problem.”1 And since they provide the sole input to subsequent stages of cortical visual processing, which in turn inform the premotor circuitry used for making eye movements, the error in measuring local velocity could be perpetuated. How are these conflicting motion signals—the potentially erroneous signals measured along a contour and the correct signals originating from terminators—ultimately resolved in the visual cortex? Microelectrode recordings from neurons in the middle temporal visual area (MT) of alert monkeys have shown that the earliest directional responses, beginning about 80 msec after the onset of stimulus motion, primarily encode the component of motion perpendicular to the orientation of a contour. That is, they are strongly affected by the ambiguous contour signals. However, the later responses (>140 msec after motion onset) encode the true direction of motion, irrespective of contour orientation. Thus the responses of MT neurons reflect the solution of the aperture problem for motion over a period of about 60 msec.2 Given the evidence that MT neuronal signals are important for the initiation of smooth pursuit eye movements,3–5 we asked whether the time-evolving signals we observed in MT neurons had a behavioral correlate. We had subjects (monkeys and humans) track the center of a single moving bar whose orientation was varied with respect to its direction of motion. The bar was dim green (4.2 cd · m−2; u′ = 0.28, v′ = 0.59), and its center was indicated by an isoluminant, red gaussian blob