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.

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).

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.

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.

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.

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.

Through the eye, slowly: delays and localization errors in the visual system.

Reviews on the visual system generally praise its amazing performance. Here we deal with its biggest weakness: sluggishness. Inherent delays lead to mislocalization when things move or, more generally, when things change.

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.

Vestibular signals can distort the perceived spatial relationship of retinal stimuli.

The flash-lag phenomenon is an illusion that affects the perceived relationship of a moving object and a briefly visible one: the moving object appears to be ahead of the flashed one. In practically all studies of this phenomenon, the image of the object moves on the retina as the object moves in space. Therefore, explanations of the illusion were sought in terms of purely visual mechanisms.

Reward-predicting and reward-detecting neuronal activity in the primate supplementary eye field.

In addition to cells specifically active with visual stimuli, saccades, or fixation, the supplementary eye field contains cells that fire in precise temporal relationship with the occurrence of reward. We studied reward-related activity in two monkeys performing a prosaccade/antisaccade task and in one monkey trained in memory prosaccades only. Two types of neurons were distinguished by their reciprocal firing pattern: reward-predicting (RP) and reward-detecting (RD).

Testing quasi-visual neurons in the monkey's frontal eye field with the triple-step paradigm.

To look successively at sites where several spots of light have appeared in the dark, we cannot simply rely on the image left by these targets on our retina. Our brain has to update target coordinates by taking into account each gaze movement that has taken place. A particular type of brain cell--the quasi-visual (QV) neuron--is assumed to play an important role in this updating by combining target coordinates and eye displacement signals.

Primate antisaccades. I. Behavioral characteristics.

The antisaccade task requires a subject to make a saccade to an unmarked location opposite to a flashed stimulus. This task was originally designed to study saccades made to a goal specified by instructions. Interest for this paradigm surged after the discovery that frontal lobe lesions specifically and severely affect human performance of antisaccades while prosaccades (i.

Interactions between natural and electrically evoked saccades. III. Is the nonstationarity the result of an integrator not instantaneously reset?

In the monkey, fixed-vector saccades evoked by superior colliculus (SC) stimulation when the animal fixates can be dramatically modified if the stimulation is applied during or immediately after an initial natural saccade. The vector is then deviated in the direction opposite to the displacement just accomplished as if it were compensating for part of the preceding trajectory. Recently, it was suggested that the amplitude of the compensatory deviation is related to the amplitude of the initial saccade linearly, and that the ratio between the two decreases exponentially as stimulation is applied later.

Interaction of the two frontal eye fields before saccade onset.

A normal environment often contains many objects of interest that compete to attract our gaze. Nevertheless, instead of initiating a flurry of conflicting signals, central populations of oculomotor neurons always seem to agree on the destination of the next saccade. How is such a consensus achieved? In a unit recording and microstimulation study on trained monkeys, we sought to elucidate the mechanism through which saccade-related cells in the frontal eye fields (FEF) avoid issuing competing commands.

Antisaccade performance predicted by neuronal activity in the supplementary eye field.

The voluntary control of gaze implies the ability to make saccadic eye movements specified by abstract instructions, as well as the ability to repress unwanted orientating to sudden stimuli. Both of these abilities are challenged in the antisaccade task, because it requires subjects to look at an unmarked location opposite to a flashed stimulus, without glancing at it. Performance on this task depends on the frontal/prefrontal cortex and related structures, but the neuronal operations underlying antisaccades are not understood.

Perceived geometrical relationships affected by eye-movement signals.

To determine the location of visual objects relative to the observer, the visual system must take account not only of the location of the stimulus on the retina, but also of the direction of gaze. In contrast, the perceived spatial relationship between visual stimuli is normally assumed to depend on retinal information alone, and not to require information about eye position. We now show, however, that the perceived alignment of three dots-tested by a vernier alignment task-is systematically altered in the period immediately preceding a saccade.

Colliding saccades evoked by frontal eye field stimulation: artifact or evidence for an oculomotor compensatory mechanism underlying double-step saccades?

What happens when the goal is changed before the movement is executed? Both the double-step and colliding saccade paradigms address this issue as they introduce a discrepancy between the retinal images of targets in space and the commands generated by the oculomotor system necessary to attain those targets. To maintain spatial accuracy under such conditions, transformations must update "retinal error' as eye position changes, and must also accommodate neural transmission delays in the system so that retinal and eye position information are temporally aligned. Different hypotheses have been suggested to account for these phenomena, based on observations of dissociable cortical and subcortical compensatory mechanisms.

The use of egocentric and exocentric location cues in saccadic programming.

Theoretically, the location of a visual target can be encoded with respect to the locations of other stimuli in the visual image (exocentric cues), or with respect to the observer (egocentric cues). Egocentric localization in the oculomotor system has been shown to rely on an internal representation of eye position that inaccurately encodes the time-course of saccadic eye movements, resulting in the mislocalization of visual targets presented near the time of a saccade. In the present investigation, subjects were instructed to localize perisaccadic stimuli in the presence or absence of a visual stimulus that could provide exocentric location information.

Illusory localization of stimuli flashed in the dark before saccades.

A photic stimulus flashed just before a saccade in the dark tends to be mislocalized in the direction of the saccade. This mislocalization is not only perceptual; it is also expressed by errors of ocular targeting. A particular situation arises if the point of light is flashed twice at the same place, the second time, just before a saccade.

Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates.

The oculomotor system has long been thought to rely on an accurate representation of eye displacement or position in a successful attempt to reconcile a stationary target's retinal instability (caused by motion of the eyes) with its corresponding spatial invariance. This is in stark contrast to perceptual localization, which has been shown to rely on a sluggish representation of eye displacement, achieving only partial compensation for the retinal displacement caused by saccadic eye movements. Recent studies, however, have begun to case doubt on the belief that the oculomotor system possess a signal of eye displacement superior to that of the perceptual system.

How the frontal eye field can impose a saccade goal on superior colliculus neurons.

Saccades were electrically evoked from the frontal eye field (FEF) of two trained monkeys while saccade-cells were recorded from the intermediate layers of the superior colliculus (SC). We found that FEF microstimulation, eliciting saccades of a given vector, excited SC saccade-cells encoding the same vector and inhibited all others. Such a mechanism can prevent competing commands from arising simultaneously in different structures.

The frontal eye field provides the goal of saccadic eye movement.

Microstimulation of oculomotor regions in primate cortex normally evokes saccadic eye movements of stereotypic directions and amplitudes. The fixed-vector nature of the evoked movements is compatible with the creation of either an artificial retinal or motor error signal. However, when microstimulation is applied during an ongoing natural saccade, the starting eye position of the evoked movement differs from the eye position at stimulation onset (due to the latency of the evoked saccade).