Sensory population decoding for visually guided movements.

We have used a new approach to study the neural decoding function that converts the population response in extrastriate area MT into estimates of target motion to drive smooth pursuit eye movement. Experiments reveal significant trial-by-trial correlations between the responses of MT neurons and the initiation of pursuit. The preponderance of significant correlations and the relatively low reduction in noise between MT and the behavioral output support the hypothesis of a sensory origin for at least some of the trial-by-trial variation in pursuit initiation. The finding of mainly positive MT-pursuit correlations, whether the target speed is faster or slower than the neuron's preferred speed, places strong constraints on the neural decoding computation. We propose that decoding is based on normalizing a weighted population vector of opponent motion responses; normalization comes from neurons uncorrelated with those used to compute the weighted population vector.

Representation of perceptually invisible image motion in extrastriate visual area MT of macaque monkeys.

Why does the world appear stable despite the visual motion induced by eye movements during fixation? We find that the answer must reside in how visual motion signals are interpreted by perception, because MT neurons in monkeys respond to the image motion caused by eye drifts in the presence of a stationary stimulus. Several features suggest a visual origin for the responses of MT neurons during fixation: spike-triggered averaging yields a peak image velocity in the preferred direction that precedes spikes by ∼60 ms; image velocity during fixation and firing rate show similar peaks in power at 4-5 Hz; and average MT firing during a period of fixation is related monotonically to the image speed along the preferred axis of the neurons 60 ms earlier. The percept caused by the responses of MT neurons during fixation depends on the distribution of activity across the population of neurons of different preferred speeds. For imposed stimulus motion, the population response peaks for neurons that prefer the actual target speed. For small image motions caused by eye drifts during fixation, the population response is large, but is noisy and does not show a clear peak. This representation of image motion in MT would be ignored if perception interprets the population response in the context of a prior of zero speed. Then, we would see a stable scene despite MT responses caused by eye drifts during fixation.

Time course of precision in smooth-pursuit eye movements of monkeys.

To evaluate the nature and possible sources of variation in sensory-motor behavior, we measured the signal-to-noise ratio for the initiation of smooth-pursuit eye movements as a function of time and computed thresholds that indicate how well the pursuit system discriminates small differences in the direction, speed, or time of onset of target motion. Thresholds improved rapidly as a function of time and came close to their minima during the interval when smooth eye movement is driven only by visual motion inputs. Many features of the data argued that motor output and sensory discrimination are limited by the same noise source. Pursuit thresholds reached magnitudes similar to those for perception: <2-3 degrees of direction, approximately 11-15% of target speed, and 8 ms of change in the time of onset of target motion. Pursuit and perceptual thresholds had similar dependencies on the duration of the motion stimulus and showed similar effects of target speed. The evolution of information about direction of target motion followed the same time course in pursuit behavior and in a previously reported sample of neuronal responses from extrastriate area MT. Changing the form of the sensory input while keeping the motor response fixed had significant effects on the signal-to-noise ratio in pursuit for direction discrimination, whereas holding the sensory input constant while changing the combination of muscles used for the motor output did not. We conclude that noise in sensory processing of visual motion provides the major source of variation in the initiation of pursuit.