Neurons that program what to do and in what order.

In this issue of Neuron, describe the activity of single neurons in the SEF of monkeys, an oculomotor area of the frontal lobe, during the performance of stereotyped sequences of saccades. The monkey had to look at one of two identical stimuli, but the only way to choose the "correct" stimulus was to learn and remember its position in each presentation of the sequence. SEF neurons could do it.

Spatial localization precedes temporal determination in visual perception.

The temporal order of two spots of light successively appearing in the dark, just before a saccade, influences their perceived spatial relation. Both spots are mislocalized in the saccade direction--the second more so than the first--because mislocalization grows as time elapses from stimulus to saccade onset. On the other hand, the perceived order of the two spots may be altered if the second spot is at the focus of spatial attention. How would these illusory perceptions of space and time interact when they are brought to play together? Could they be independent or could one perception depend on the other? Here we show that perceived location of stimuli is not affected by illusory temporal order, whereas perceived temporal order is affected by misperceived location. The results suggest that the brain processes spatial location of visual stimuli before processing their temporal order.

Visuo-motor control: when the brain loses track of the eyes.

In single-units studies, neuronal signals are recorded to assess their significance and, hopefully, their role in controlling behavior. A new study of neuronal signals associated with eye position helps to explain not only how the system normally works, but also how it sometimes fails.

Video game for monkeys.

Recent progress in neurophysiological recording has developed in two directions. One relies on multimicroelectrodes to study correlations in neuron firing. The other relies on sophisticated tasks to distinguish successive stages of neuronal processing. In this issue of Neuron, Shichinohe et al. take this second approach to analyze neuronal mechanisms of pursuit.

Transfer of learned perception of sensorimotor simultaneity.

Synchronizing a motor response to a predictable sensory stimulus, like a periodic flash or click, relies on feedback (somesthetic, auditory, visual, or other) from the motor response. Practically, this results in a small (<50 ms) asynchrony in which the motor response leads the sensory event. Here we show that the perceived simultaneity in a coincidence-anticipation task (line crossing) is affected by changing the perceived simultaneity in a different task (pacing). In the pace task, human subjects were instructed to press a key in perfect synchrony with a red square flashed every second. In training sessions, feedback was provided by flashing a blue square with each key press, below the red square. There were two types of training pace sessions: one in which the feedback was provided with no delay, the other (adapting), in which the feedback was progressively delayed (up to 100 ms). Subjects' asynchrony was unchanged in the first case, but it was significantly increased in the pace task with delay. In the coincidence-anticipation task, a horizontally moving vertical bar crossed a vertical line in the middle of a screen. Subjects were instructed to press a key exactly when the bar crossed the line. They were given no feedback on their performance. Asynchrony on the line-crossing task was tested after the training pace task with feedback. We found that this asynchrony to be significantly increased even though there never was any feedback on the coincidence-anticipation task itself. Subjects were not aware that their sensorimotor asynchrony had been lengthened (sometimes doubled). We conclude that perception of simultaneity in a sensorimotor task is learned. If this perception is caused by coincidence of signals in the brain, the timing of these signals depends on something-acquired by experience-more adaptable than physiological latencies.

Frames of reference for saccadic command tested by saccade collision in the supplementary eye field.

In what frame of reference does the supplementary eye field (SEF) encode saccadic eye movements? In this study, the "saccade collision" test was used to determine whether a saccade electrically evoked in the monkey's SEF is programmed to reach an oculocentric goal or a nonoculocentric (e.g., head or body-centered) goal. If the eyes start moving just before or when an oculocentric goal is imposed by electrical stimulation, the trajectory of the saccade to that goal should compensate for the ongoing movement. Conversely, if the goal imposed by electrical stimulation is nonoculocentric, the trajectory of the evoked saccade should not be altered. In head-fixed experiments, we mapped the trajectories of evoked saccades while the monkey fixated at each of 25 positions 10 degrees apart in a 40 x 40 degrees grid. For each studied SEF site, we calculated convergences indices and found that "convergent" and "nonconvergent" sites were separately clustered: nonconvergent rostral to convergent. Then, the "saccade collision" test was systematically applied. We found compensation at sites where saccades were of the nonconvergent type and practically no compensation at sites where saccades were of the convergent type. The results indicate that the SEF can encode saccade goals in at least two frames of reference and suggest a rostrocaudal segregation in the representation of these two modes.

Voluntary action expands perceived duration of its sensory consequence.

When we look at a clock with a hand showing seconds, the hand sometimes appears to stay longer at its first-seen position than at the following positions, evoking an illusion of chronostasis. This illusory extension of perceived duration has been shown to be coupled to saccadic eye movement and it has been suggested to serve as a mechanism of maintaining spatial stability across the saccade. Here, we examined the effects of three kinds of voluntary movements on the illusion of chronostasis: key press, voice command, and saccadic eye movement. We found that the illusion can occur with all three kinds of voluntary movements if such movements start the clock immediately. When a delay is introduced between the voluntary movement and the start of the clock, the delay itself is overestimated. These results indicate that the illusion of chronostasis is not specific to saccadic eye movement, and may therefore involve a more general mechanism of how voluntary action influences time perception.

Primate antisaccade. II. Supplementary eye field neuronal activity predicts correct performance.

Neuronal activities were recorded in the supplementary eye field (SEF) of 3 macaque monkeys trained to perform antisaccades pseudorandomly interleaved with prosaccades, as instructed by the shape of a central fixation point. The prosaccade goal was indicated by a peripheral stimulus flashed anywhere on the screen, whereas the antisaccade goal was an unmarked site diametrically opposite the flashed stimulus. The visual cue was given immediately after the instruction cue disappeared in the immediate-saccade task, or during the instruction period in the delayed-saccade task. The instruction cue offset was the saccade gosignal. Here we focus on 92 task-related neurons: visual, eye-movement, and instruction/fixation neurons. We found that 73% of SEF eye-movement-related neurons fired significantly more before anti-saccades than prosaccades. This finding was analyzed at 3 levels: population, single neuron, and individual trial. On individual antisaccade trials, 40 ms before saccade, the firing rate of eye-movement-related neurons was highly predictive of successful performance. A similar analysis of visual responses (40 ms astride the peak) gave less-coherent results. Fixation neurons, activated during the initial instruction period (i.e., after the instruction cue but before the stimulus) always fired more on antisaccade than on prosaccade trials. This trend, however, was statistically significant for only half of these neurons. We conclude that the SEF is critically involved in the production of antisaccades.