Neurons in cortical area MST remap the memory trace of visual motion across saccadic eye movements

Perception of a stable visual world despite eye motion requires integration of visual information across saccadic eye movements. To investigate how the visual system deals with localization of moving visual stimuli across saccades, we observed spatiotemporal changes of receptive fields (RFs) of motion-sensitive neurons across periods of saccades in the middle temporal (MT) and medial superior temporal (MST) areas. We found that the location of the RFs moved with shifts of eye position due to saccades, indicating that motion-sensitive neurons in both areas have retinotopic RFs across saccades. Different characteristic responses emerged when the moving visual stimulus was turned off before the saccades. For MT neurons, virtually no response was observed after the saccade, suggesting that the responses of these neurons simply reflect the reafferent visual information. In contrast, most MST neurons increased their firing rates when a saccade brought the location of the visual stimulus into their RFs, where the visual stimulus itself no longer existed. These findings suggest that the responses of such MST neurons after saccades were evoked by a memory of the stimulus that had preexisted in the postsaccadic RFs (“memory remapping”). A delayed-saccade paradigm further revealed that memory remapping in MST was linked to the saccade itself, rather than to a shift in attention. Thus, the visual motion information across saccades was integrated in spatiotopic coordinates and represented in the activity of MST neurons. This is likely to contribute to the perception of a stable visual world in the presence of eye movements.The inhomogeneous visual resolution of the retina requires eye motion by saccadic eye movements to look around the environment. However, despite the frequent occurrences of saccades, humans are able to perceive the visual world as stable and continuous. Because each saccade changes the retinal locations of visual objects in the external world, the retinotopic representation of the visual scene in the brain must be overwritten by a new one according to each new eye position. One possible solution for the visual system to overcome such repetitions and to maintain perceptual continuity across saccades is to integrate the visual information before and after eye movement. As the neuronal correlate of the integration across saccades, so-called “remapping” of the visual scene has been reported in several visual areas, including the lateral intraparietal cortex (LIP), frontal eye field (FEF), and superior colliculus (SC). This emphasizes the predictive shift of the receptive field (RF) of the neuron to the location into which the developing saccade would bring the stimulus (1–6). However, the changes of the spatiotemporal characteristics of the RF have yet to be explored and are essential information for understanding the integration across the period of saccades.To examine how the visual system deals with localization of moving visual stimuli across saccades, we carried out continuous observation of the RFs of neurons in the motion-sensitive cortical areas of monkeys: the middle temporal (MT) and medial superior temporal (MST) areas (7). Single-unit activities were recorded while the animals performed fixation and saccade tasks in which a spatially stable moving stimulus was presented in various visual fields. The moving stimulus was presented for long (600 ms) and short (170 ms) durations to allow observation of spatiotemporal RF maps throughout the period of saccades and to examine possible RF-remapping across saccades, respectively.     

Demonstration of artificial visual percepts generated through thalamic microstimulation

Electrical stimulation of the visual system might serve as the foundation for a prosthetic device for the blind. We examined whether microstimulation of the dorsal lateral geniculate nucleus of the thalamus can generate localized visual percepts in alert monkeys. To assess electrically generated percepts, an eye-movement task was used with targets presented on a computer screen (optically) or through microstimulation of the lateral geniculate nucleus (electrically). Saccades (fast, direct eye movements) made to electrical targets were comparable to saccades made to optical targets. Gaze locations for electrical targets were well predicted by measured visual response maps of cells at the electrode tips. With two electrodes, two distinct targets could be independently created. A sequential saccade task verified that electrical targets were processed not in motor coordinates, but in visual spatial coordinates. Microstimulation produced predictable visual percepts, showing that this technique may be useful for a visual prosthesis.     

Correspondence of presaccadic activity in the monkey primary visual cortex with saccadic eye movements

We continuously scan the visual world via rapid or saccadic eye movements. Such eye movements are guided by visual information, and thus the oculomotor structures that determine when and where to look need visual information to control the eye movements. To know whether visual areas contain activity that may contribute to the control of eye movements, we recorded neural responses in the visual cortex of monkeys engaged in a delayed figure-ground detection task and analyzed the activity during the period of oculomotor preparation. We show that approximately 100 ms before the onset of visually and memory-guided saccades neural activity in V1 becomes stronger where the strongest presaccadic responses are found at the location of the saccade target. In addition, in memory-guided saccades the strength of presaccadic activity shows a correlation with the onset of the saccade. These findings indicate that the primary visual cortex contains saccade-related responses and participates in visually guided oculomotor behavior.     

Dynamic sensitivity of area V4 neurons during saccade preparation

During the preparation of saccadic eye movements, visual attention is confined to the target of intended fixation and there is a corresponding diminution of visual sensitivity at nontarget locations. Neurons within the macaque visual cortex exhibit correlates of these perceptual changes, such as in area V4, where neuronal responses are enhanced during the preparation of saccades to stimuli within the receptive field (RF), and responses are suppressed during the preparation of saccades to other locations. Both the perceptual and neurophysiological effects suggest that the sensitivity of visual cortical neurons to input is dynamic during saccade preparation. We probed the contrast sensitivity of area V4 neurons to nontarget stimuli at varying times during the preparation of saccades to locations outside of the neuron''s receptive field. We found that the contrast sensitivity of many neurons is profoundly altered within 50 ms of saccade onset. The luminance or color contrast sensitivity of individual V4 neurons could increase, decrease, or remain unchanged before saccade onset. For luminance contrast sensitivity, decreases in sensitivity were more frequent and larger in magnitude, resulting in an overall decrement in sensitivity across the population. For color contrast, the effects were smaller and more heterogeneous, resulting in little or no overall change in sensitivity across the population. Our results demonstrate the dynamic influence that saccade preparation has on the sensitivity of visual cortical neurons and suggest a basis for the changes in perception known to occur during saccade preparation.     

Neural correlates of goal-directed and non–goal-directed movements

What are the cortical neural correlates that distinguish goal-directed and non–goal-directed movements? We investigated this question in the monkey frontal eye field (FEF), which is implicated in voluntary control of saccades. Here, we compared FEF activity associated with goal-directed (G) saccades and non–goal-directed (nG) saccades made by the monkey. Although the FEF neurons discharged before these nG saccades, there were three major differences in the neural activity: First, the variability in spike rate across trials decreased only for G saccades. Second, the local field potential beta-band power decreased during G saccades but did not change during nG saccades. Third, the time from saccade direction selection to the saccade onset was significantly longer for G saccades compared with nG saccades. Overall, our results reveal unexpected differences in neural signatures for G versus nG saccades in a brain area that has been implicated selectively in voluntary control. Taken together, these data add critical constraints to the way we think about saccade generation in the brain.

Many movements are goal-directed while others, such as fidgets, may not be. However, the differences between the neural mechanisms that control these different movements are poorly understood. The macaque frontal eye field (FEF) in particular has neurons that discharge before visually guided saccades and saccades made in total darkness such as learned saccades or memory-guided saccades (1) but not before spontaneous saccades in total darkness (2). Here, we discovered that when monkeys make saccades that have no obvious goal, in a lit environment, FEF movement and visuomovement neurons do, in fact, discharge. We asked if there were any differences in neural activities that distinguished non–goal-directed (nG) saccades from goal-directed (G) saccades.We studied two characteristics of neural response not directly visible in the firing rate but which precede movements: a decrease in neural response variability (3) and a decrease in local field potential (LFP) beta oscillatory activity (4, 5). Previous studies have shown that decreases in response variability are correlated with attention (6), planning of saccades (3, 7, 8), the onset of a visual stimulus (3, 9), and the amount of expected reward (10), among other processes. Decreases in beta power have been correlated with motor preparation and inhibitory control (11, 12), among other processes (13). Nevertheless, despite these efforts, their roles in goal-directed versus non–goal-directed movement generation have not been studied.Here, we studied simultaneously recorded neural spiking and LFP in the FEF in the primate frontal cortex and show evidence for differential cortical control for G and nG saccades: Although FEF saccade-related neurons do discharge before nG saccades, we found that for G saccades, but not for nG saccades, the variability in spike rate across trials decreased, and there was a concurrent reduction of LFP beta-band power. Furthermore, the time from saccade direction selection to saccade onset was significantly longer for G saccades compared with nG saccades.     

Correlates of transsaccadic integration in the primary visual cortex of the monkey

We make several eye movements per second when we explore a visual scene. Each eye movement sweeps the scene's projection across the retina and changes its representation in retinotopic areas of the visual cortex, but we nevertheless perceive a stable world. Here we investigate the neuronal correlates of visual stability in the primary visual cortex. Monkeys were trained to make two saccades along a single curve and to ignore another, distracting curve. Attention enhanced neuronal responses to the entire relevant curve before the first saccade. This response enhancement was rapidly reestablished after the saccade, although the image was shifted across the primary visual cortex. We argue that this fast postsaccadic restoration of the attentional response enhancement contributes to the stability of vision across eye movements, and reduces the impact of saccades on visual cognition.     

An oculomotor representation area within the ventral premotor cortex

We explored the ventral part of the premotor cortex (PMV) with intracortical microstimulation (ICMS) while monkeys performed a visual fixation task, to see whether the PMV is involved in oculomotor control. ICMS evoked saccades from a small-restricted region in the PMV, without evoking movements in the limbs, neck, or body. We found the saccade-evoking site in the PMV in a total of three hemispheres in two monkeys. Quantitative analysis of the effects of eye position on saccades evoked by microstimulation of the PMV characterized the evoked saccades as goal directed. The nature of the saccades evoked in the PMV contrasted with the fixed vector nature of saccades evoked by ICMS of the frontal eye field. We also found that neurons in this restricted area of the PMV were active while the animals were performing a saccade task that required them to make saccades toward targets without arm movements. These data provide evidence for the presence of an oculomotor-specific subregion within the PMV. This subregion and the surrounding skeletomotor-representing regions of the PMV seem to coordinate oculomotor and skeletomotor control in performing goal-directed motor tasks.     

Dissociation of spatial attention and saccade preparation

The goal of this experiment was to determine whether the allocation of attention necessarily requires saccade preparation. To dissociate the focus of attention from the endpoint of a saccade, macaque monkeys were trained to perform visual search for a uniquely colored rectangle and shift gaze either toward or opposite this color singleton according to its orientation. A vertical singleton cued a prosaccade, a horizontal singleton, an antisaccade. Saccade preparation was probed by measuring the direction of saccades evoked by intracortical microstimulation of the frontal eye fields at variable times after presentation of the search array. Eye movements evoked on prosaccade trials deviated progressively toward the singleton that was also the endpoint of the correct eye movement. However, eye movements evoked on antisaccade trials never deviated toward the singleton but only progressively toward the location opposite the singleton. This occurred even though previous work showed that on antisaccade trials most neurons in frontal eye fields initially select the singleton while attention is allocated to distinguish its shape. Thus, sensorimotor structures can covertly orient attention without preparing a saccade.     

The time course of visual information accrual guiding eye movement decisions

Saccadic eye movements are the result of neural decisions about where to move the eyes. These decisions are based on visual information accumulated before the saccade; however, during an ≈100-ms interval immediately before the initiation of an eye movement, new visual information cannot influence the decision. Does the brain simply ignore information presented during this brief interval or is the information used for the subsequent saccade? Our study examines how and when the brain integrates visual information through time to drive saccades during visual search. We introduce a new technique, saccade-contingent reverse correlation, that measures the time course of visual information accrual driving the first and second saccades. Observers searched for a contrast-defined target among distractors. Independent contrast noise was added to the target and distractors every 25 ms. Only noise presented in the time interval in which the brain accumulates information will influence the saccadic decisions. Therefore, we can retrieve the time course of saccadic information accrual by averaging the time course of the noise, aligned to saccade initiation, across all trials with saccades to distractors. Results show that before the first saccade, visual information is being accumulated simultaneously for the first and second saccades. Furthermore, information presented immediately before the first saccade is not used in making the first saccadic decision but instead is stored and used by the neural processes driving the second saccade.Saccadic eye movements are used to reorient the line of sight of the fovea to explore objects of interest. Each saccade is the result of a neural decision that is based on the processing of visual information. Neural activity related to motor preparation and visual selection has been measured in different brain areas before saccade execution (1-4); however, it is still unknown when and how the brain accumulates visual information used to choose the destination of each saccade. Immediately before each saccade''s execution, as a consequence of sensory transduction and motor pathway delays (5), there is a “dead time,” an ≈100-ms time interval in which visual information does not influence the destination of the saccade. What is the impact of this on performance and strategy in a search task? Searching for an object in a scene typically requires a sequence of several saccades. If each saccade were based on a concatenation of separate independent neural decisions, each with its own dead time, then searching a complex scene would be very inefficient and difficult. Instead, for some conditions, it appears that a fast sequence of saccades is programmed in parallel (6-12). Subsequent saccadic latencies can be very short compared with the initial saccade''s latency (7, 8), and in some cases the second saccade even disregards visual information presented after the execution of the first saccade (10, 11). Recently, a study measuring neural activity in the superior colliculus of monkeys provided evidence that for sequences of fast saccades, motor activity related to the goal of a second saccade can temporally overlap with activity related to an initial saccade (13). However, the time course of how the brain weights and accumulates visual information used to guide the first and second saccades is still unknown.Correlating human perceptual decisions with stimuli containing external noise can elucidate the mechanisms mediating decisions and actions (14-17). This technique, referred to as “reverse correlation” or “classification images,” has been used to study the mechanisms humans use to process spatial (18-20) and temporal (21, 22) visual information. This method uses noise features that led to incorrect decisions, to retrieve the weights that an observer used to integrate visual information. Here, we record human eye movements during visual search for a bright target among distractors and use the temporal reverse correlation technique aligned to saccade initiation to measure how the saccadic system integrates visual information over time. In our experiments, the contrast of the target and the distractors varied through time because of statistically independent temporal noise. Noise making a distractor brighter than the target will tend to lead observers to make an incorrect saccade to that distractor. The logic of the current experiment is that a saccade will be affected only by noise presented during the time in which the brain integrates information and not by noise presented during the dead time before saccadic execution. Thus, by averaging over trials the time series of noise values presented at the distractor location selected by the saccadic eye movement, we will obtain a profile of the temporal window in which the brain accumulates visual information for eye movements during a search.     

Anticipating the three-dimensional consequences of eye movements

Rapid eye movements called saccades give rise to sudden, enormous changes in optic information arriving at the eye; how the world nonetheless appears stable is known as the problem of spatial constancy. One consequence of saccades is that the directions of all visible points shift uniformly; directional or 2D constancy, the fact that we do not perceive this change, has received extensive study for over a century. The problems raised by 3D consequences of saccades, on the other hand, have been neglected. When the eye rotates in space, the 3D orientation of all stationary surfaces undergoes an equal-and-opposite rotation with respect to the eye. When presented with a an optic simulation of a saccade but with the eyes still, observers readily perceive this depth rotation of surfaces; when simultaneously performing the corresponding saccade, the 3D orientations of surfaces are perceived as stable, a phenomenon I propose calling 3D spatial constancy. In experiments presented here, observers viewed ambiguous 3D rotations immediately before, during, or after a saccade. The results show that before the eyes begin to move the brain anticipates the 3D consequences of saccades, preferring to perceive the rotation opposite to the impending eye movement. Further, the anticipation is absent when observers fixate while experiencing optically simulated saccades, and therefore must be evoked by extraretinal signals. Such anticipation could provide a mechanism for 3D spatial constancy and transsaccadic integration of depth information.     

Motion perception of saccade-induced retinal translation

Active visual perception relies on the ability to interpret correctly retinal motion signals induced either by moving objects viewed with static eyes or by stationary objects viewed with moving eyes. A motionless environment is not normally perceived as moving during saccadic eye movements. It is commonly believed that this phenomenon involves central oculomotor signals that inhibit intrasaccadic visual motion processing. The keystone of this extraretinal theory relies on experimental reports showing that physically stationary scenes displayed only during saccades, thus producing high retinal velocities, are never perceived as moving but appear as static blurred images. We, however, provide evidence that stimuli optimized for high-speed motion detection elicit clear motion perception against saccade direction, thus making the search for extraretinal suppression superfluous. The data indicate that visual motion is the main cue used by observers to perform the task independently of other perceptual factors covarying with intrasaccadic stimulation. By using stimuli of different durations, we show that the probability of perceiving the stimulus as static, rather than moving, increases when the intrasaccadic stimulation is preceded or followed by a significant extrasaccadic stimulation. We suggest that intrasaccadic motion perception is accomplished by motion-selective magnocellular neurons through temporal integration of rapidly increasing retinal velocities. The functional mechanism that usually prevents this intrasaccadic activity from being perceived seems to rely on temporal masking effects induced by the static retinal images present before and/or after the saccade.     

Deficits in eye movement control in children with fetal alcohol spectrum disorders

BACKGROUND: Prenatal exposure to alcohol can result in a spectrum of adverse developmental outcomes in offspring, collectively termed fetal alcohol spectrum disorders (FASD). Deficits in executive function--the psychological processes involved in controlling voluntary goal-oriented behavior--are prevalent in FASD. Oculomotor tasks have been designed as highly sensitive tools to evaluate components of executive function. Because of the extensive overlap in the brain areas controlling eye movements and those affected in FASD, we hypothesized that individuals with FASD display specific neurobehavioral abnormalities that can be quantified with eye movement testing. METHODS: Subjects (8-12 years old) were instructed to look either toward (prosaccade) or away from (antisaccade) a stimulus that appeared in the peripheral visual field. Two fixation conditions were used. In the gap condition, the central fixation point (FP) was removed before the appearance of the peripheral stimulus; in the overlap condition, the FP remained illuminated. Saccadic reaction times (SRTs, time from stimulus appearance to saccade initiation), direction errors (saccades made in the incorrect direction relative to instruction), and express saccades (short-latency: SRT=90-140 ms) were measured to assess automatic and volitional saccade control. RESULTS: Compared with controls, FASD children had elongated reaction times, excessive direction errors, and no express saccades. Metric analysis of correct prosaccades revealed a trend toward increased saccadic duration and decreased saccadic velocity in FASD subjects. CONCLUSION: These results reflect deficits in executive function and motor control, and are consistent with dysfunction of the frontal lobes, possibly due to disrupted inhibitory mechanisms. Therefore, eye movement tasks may be powerful and easy tools for assessing executive function deficits in FASD.     

Neural mechanisms underlying the temporal control of sequential saccade planning in the frontal eye field

Sequences of saccadic eye movements are instrumental in navigating our visual environment. While neural activity has been shown to ramp up to a threshold before single saccades, the neural underpinnings of multiple saccades is unknown. To understand the neural control of saccade sequences, we recorded from the frontal eye field (FEF) of macaque monkeys while they performed a sequential saccade task. We show that the concurrent planning of two saccade plans brings forth processing bottlenecks, specifically by decreasing the growth rate and increasing the threshold of saccade-related ramping activity. The rate disruption affected both saccade plans, and a computational model, wherein activity related to the two saccade plans mutually and asymmetrically inhibited each other, predicted the behavioral and neural results observed experimentally. Borrowing from models in psychology, our results demonstrate a capacity-sharing mechanism of processing bottlenecks, wherein multiple saccade plans in a sequence compete for the processing capacity by the perturbation of the saccade-related ramping activity. Finally, we show that, in contrast to movement-related neurons, visual activity in FEF neurons is not affected by the presence of multiple saccade targets, indicating that, for perceptually simple tasks, inhibition within movement-related neurons mainly instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.

Saccadic eye movements shift the fovea from one point to another, serially sampling our visual surroundings and aiding consequent behavior. Proper planning and execution of saccade sequences is essential for performing everyday tasks such as reading. Despite extensive research on the neural basis of planning individual saccades, the neural mechanisms underlying the sequencing of multiple saccades remain largely unknown. Previous research has shown that sequential saccades can be processed in parallel (1–15). Sequential saccade studies have shown that, as the temporal gap between the targets (target step delay; TSD) decreases, the latency of the response to the second stimulus increases markedly, as if the brain inherently cannot process two simple decisions at the same time (16, 17). The bottlenecks associated with parallel programming of multiple saccade plans form the basis of this study.Various theoretical frameworks have been proposed to explain how closely spaced action plans interfere with each other. Single-channel bottleneck models propose that a central, decision-making stage constitutes the bottleneck, wherein the central stages of multiple plans can only proceed serially and cannot be “coactive” (16, 18–20). For a sequence of two saccades, the first plan is likely to reach the central stage first, and thus, the saccade 2 plan must “wait” until central processing of the first is over (Fig. 1A). In contrast, capacity-sharing models argue that the decision-making stages of both plans can proceed in parallel, albeit with differential rates. The concept of the brain’s “capacity” corresponds to the brain’s general information–processing capabilities (21–24), independent of task type. The capacity-sharing models predict that, because of its temporal precedence, the first saccade plan will get the major share of the capacity, and the second saccade plan will get a smaller fraction, thus delaying the onset of the second response (Fig. 1B; 25, 26).Open in a separate windowFig. 1.Behavioral predictions for processing bottlenecks during the planning of sequential saccades. (A) Single-channel bottleneck framework. Each task is made up of three stages. The visual stage (V) can be carried on in parallel with stages of another task, but the central planning stage, P, can only proceed serially. In a two-saccade sequence, the stages of the first saccade plan proceed to completion unabated, leading to its execution (E). For the second plan, however, if the second target closely follows the first (short TSD condition), the central planning stage, P2, is postponed until P1 is complete. Such a postponement does not occur in the long TSD condition, in which the two saccade plans are well separated, thereby leading to an increase of RT2 from long to short TSD. (B) Capacity-sharing bottleneck framework. In this framework, the P stages of multiple plans can proceed in parallel and access the brain’s limited processing capacity simultaneously. In the short TSD condition, P1 and P2 concurrently “share” the capacity, resulting in the slower progress of both saccade plans. This leads to the lengthening of both RT1 and RT2 in the short TSD condition, the effect on RT2 being greater as the second saccade plan gets a smaller share of the central capacity. (C) Predictions of reaction time versus TSD for single-channel bottleneck framework (Left) and capacity-sharing bottleneck framework (Right). RT2 increases with the decrease in TSD for both frameworks, whereas RT1 increase is predicted only by the capacity-sharing model. (D) Behavioral data for reaction time versus TSD. Data shows trials in which the first (for RT1) or second (for RT2) saccade was into the RF. Both reaction times increased significantly with the decrease in TSD. T1, T2, S1, S2 refer to the onsets of the first target, second target, first saccade, and second saccade, respectively. ***P < 0.001, **P < 0.01.The neural mechanisms of processing bottlenecks in sequential saccade planning are not known. To investigate the neural architecture of saccade-related bottlenecks, we recorded from the frontal eye field (FEF) of macaque monkeys performing a sequential saccade task. FEF is a good candidate region to study the neural imprints of processing bottlenecks, since it is a higher-order control center for goal-directed saccadic planning (27–29). Furthermore, the activity of FEF movement neurons follow the dynamics of accumulator models and resemble the central, capacity-limited stage observed in computational models of dual-task studies (30–32). Finally, FEF movement neurons can encode two saccade plans in parallel (4), and thus, any limitations arising during the concurrent programming of saccades may be found in the activity of movement-related neurons in the FEF (4).In this study, we show that FEF movement neurons constitute a bottleneck locus—the processing of saccadic sequences is slowed down by reducing the speed of activity growth or by increasing movement activation threshold. Such adjustments were observed for both the first and second saccade plans, indicating that a capacity-sharing mechanism might underlie temporal delays that limit the extent of parallel processing seen during the sequencing of multiple actions.     

Identity of a pathway for saccadic suppression

Neurons in the superficial gray layer (SGS) of the superior colliculus receive visual input and excite intermediate layer (SGI) neurons that play a critical role in initiating rapid orienting movements of the eyes, called saccades. In the present study, two types of experiments demonstrate that a population of SGI neurons gives rise to a reciprocal pathway that inhibits neurons in SGS. First, in GAD67-GFP knockin mice, GABAergic SGI neurons that expressed GFP fluorescence were injected with the tracer biocytin to reveal their axonal projections. Axons arising from GFP-positive neurons in SGI terminated densely in SGS. Next, SGI neurons in rats and mice were stimulated by using the photolysis of caged glutamate, and in vitro whole-cell patch-clamp recordings were used to measure the responses evoked in SGS cells. Large, synaptically mediated outward currents were evoked in SGS neurons. These currents were blocked by gabazine, confirming that they were GABA(A) receptor-mediated inhibitory postsynaptic currents. This inhibitory pathway from SGI transiently suppresses visual activity in SGS, which in turn could have multiple effects. These effects could include reduction of perceptual blurring during saccades as well as prevention of eye movements that might be spuriously triggered by the sweep of the visual field across the retina.     

A neural network model of sensoritopic maps with predictive short-term memory properties.

Coordinated orienting movements can be accurately performed without direct sensory control. Ocular saccades, for instance, have been shown to be reprogrammed after target disappearance when an intervening eye movement is electrically triggered before the saccade onset. Saccadic eye movements can also be executed toward memorized targets, even when the subject has been passively moved in darkness. Two hypotheses have been proposed to account for this goal-invariance property: either (i) the goal is reconstructed and memorized in the stable frame of reference linked to the environment ("allocentric, coordinates") or (ii) the goal is selected and memorized in the sensors-related maps ("egocentric coordinates") and is continuously updated by efferent copies of the motor commands. In this paper, we shall describe a formal neural network based on this second hypothesis. The results of the simulation show that target position can be memorized and accurately updated in a topologically ordered map, using a velocity-signal feedback. Moreover, this network has been submitted to a simple learning procedure by using the intermittent visual recurring afferent signal as the teaching signal. A similar mechanism could be involved in control of limb movement.     

Parietal stimulation destabilizes spatial updating across saccadic eye movements

Saccadic eye movements cause sudden and global shifts in the retinal image. Rather than causing confusion, however, eye movements expand our sense of space and detail. In macaques, a stable representation of space is embodied by neural populations in intraparietal cortex that redistribute activity with each saccade to compensate for eye displacement, but little is known about equivalent updating mechanisms in humans. We combined noninvasive cortical stimulation with a double-step saccade task to examine the contribution of two human intraparietal areas to transsaccadic spatial updating. Right hemisphere stimulation over the posterior termination of the intraparietal sulcus (IPSp) broadened and shifted the distribution of second-saccade endpoints, but only when the first-saccade was directed into the contralateral hemifield. By interleaving trials with and without cortical stimulation, we show that the shift in endpoints was caused by an enduring effect of stimulation on neural functioning (e.g., modulation of neuronal gain). By varying the onset time of stimulation, we show that the representation of space in IPSp is updated immediately after the first-saccade. In contrast, stimulation of an adjacent IPS site had no such effects on second-saccades. These experiments suggest that stimulation of IPSp distorts an eye position or displacement signal that updates the representation of space at the completion of a saccade. Such sensory-motor integration in IPSp is crucial for the ongoing control of action, and may contribute to visual stability across saccades.     

Compression of auditory space during rapid head turns

Studies of spatial perception during visual saccades have demonstrated compressions of visual space around the saccade target. Here we psychophysically investigated perception of auditory space during rapid head turns, focusing on the "perisaccadic" interval. Using separate perceptual and behavioral response measures we show that spatial compression also occurs for rapid head movements, with the auditory spatial representation compressing by up to 50%. Similar to observations in the visual system, this occurred only when spatial locations were measured by using a perceptual response; it was absent for the behavioral measure involving a nose-pointing task. These findings parallel those observed in vision during saccades and suggest that a common neural mechanism may subserve these distortions of space in each modality.     

Updating of the visual representation in monkey striate and extrastriate cortex during saccades

Neurons in the lateral intraparietal area, frontal eye field, and superior colliculus exhibit a pattern of activity known as remapping. When a salient visual stimulus is presented shortly before a saccade, the representation of that stimulus is updated, or remapped, at the time of the eye movement. This updating is presumably based on a corollary discharge of the eye movement command. To investigate whether visual areas also exhibit remapping, we recorded from single neurons in extrastriate and striate cortex while monkeys performed a saccade task. Around the time of the saccade, a visual stimulus was flashed either at the location occupied by the neuron's receptive field (RF) before the saccade (old RF) or at the location occupied by it after the saccade (new RF). More than half (52%) of V3A neurons responded to a stimulus flashed in the new RF even though the stimulus had already disappeared before the saccade. These neurons responded to a trace of the flashed stimulus brought into the RF by the saccade. In 16% of V3A neurons, remapped activity began even before saccade onset. Remapping also was observed at earlier stages of the visual hierarchy, including in areas V3 and V2. At these earlier stages, the proportion of neurons that exhibited remapping decreased, and the latency of remapped activity increased relative to saccade onset. Remapping was very rare in striate cortex. These results indicate that extrastriate visual areas are involved in the process of remapping.     

Proactive control of sequential saccades in the human supplementary eye field

Our ability to regulate behavior based on past experience has thus far been examined using single movements. However, natural behavior typically involves a sequence of movements. Here, we examined the effect of previous trial type on the concurrent planning of sequential saccades using a unique paradigm. The task consisted of two trial types: no-shift trials, which implicitly encouraged the concurrent preparation of the second saccade in a subsequent trial; and target-shift trials, which implicitly discouraged the same in the next trial. Using the intersaccadic interval as an index of concurrent planning, we found evidence for context-based preparation of sequential saccades. We also used functional MRI-guided, single-pulse, transcranial magnetic stimulation on human subjects to test the role of the supplementary eye field (SEF) in the proactive control of sequential eye movements. Results showed that (i) stimulating the SEF in the previous trial disrupted the previous trial type-based preparation of the second saccade in the nonstimulated current trial, (ii) stimulating the SEF in the current trial rectified the disruptive effect caused by stimulation in the previous trial, and (iii) stimulating the SEF facilitated the preparation of second saccades based on previous trial type even when the previous trial was not stimulated. Taken together, we show how the human SEF is causally involved in proactive preparation of sequential saccades.     

Techniques of determining saccadic parameters

For the analysis of saccadic eye movements two values were to be computed: the latency of the reaction and the maximum velocity reached by the eye finding the new visual point. The waveform is disturbed especially by noise. With this method, the impurity level can be reduced nearly completely without destroying the curve shape of the saccade.