11505398
Corollary discharge contributes to perceived eye location in monkeys.
Despite saccades changing the image on the retina several times per second, we still perceive a stable visual world. A possible mechanism underlying this stability is that an internal retinotopic map is updated with each saccade, with the location of objects being compared before and after the saccade. Psychophysical experiments have shown that humans derive such location information from a corollary discharge (CD) accompanying saccades. Such a CD has been identified in the monkey brain in a circuit extending from superior colliculus to frontal cortex. There is a missing piece, however. Perceptual localization is established only in humans and the CD circuit only in monkeys. We therefore extended measurement of perceptual localization to the monkey by adapting the target displacement detection task developed in humans. During saccades to targets, the target disappeared and then reappeared, sometimes at a different location. The monkeys reported the displacement direction. Detections of displacement were similar in monkeys and humans, but enhanced detection of displacement from blanking the target at the end of the saccade was observed only in humans, not in monkeys. Saccade amplitude varied across trials, but the monkey's estimates of target location did not follow that variation, indicating that eye location depended on an internal CD rather than external visual information. We conclude that monkeys use a CD to determine their new eye location after each saccade, just as humans do.
36982480
The updating of the representation of visual space in parietal cortex by intended eye movements.
Every eye movement produces a shift in the visual image on the retina. The receptive field, or retinal response area, of an individual visual neuron moves with the eyes so that after an eye movement it covers a new portion of visual space. For some parietal neurons, the location of the receptive field is shown to shift transiently before an eye movement. In addition, nearly all parietal neurons respond when an eye movement brings the site of a previously flashed stimulus into the receptive field. Parietal cortex both anticipates the retinal consequences of eye movements and updates the retinal coordinates of remembered stimuli to generate a continuously accurate representation of visual space.
18080
Neuronal mechanisms of visual stability
Human vision is stable and continuous in spite of the incessant interruptions produced by saccadic eye movements. These rapid eye movements serve vision by directing the high resolution fovea rapidly from one part of the visual scene to another. They should detract from vision because they generate two major problems: displacement of the retinal image with each saccade and blurring of the image during the saccade. This review considers the substantial advances in understanding the neuronal mechanisms underlying this visual stability derived primarily from neuronal recording and inactivation studies in the monkey, an excellent model for systems in the human brain. For the first problem, saccadic displacement, two neuronal candidates are salient. First are the neurons in frontal and parietal cortex with shifting receptive fields that provide anticipatory activity with each saccade and are driven by a corollary discharge. These could provide the mechanism for a retinotopic hypothesis of visual stability and possibly for a transsaccadic memory hypothesis, The second neuronal mechanism is provided by neurons whose visual response is modulated by eye position (gain field neurons) or are largely independent of eye position (real position neurons), and these neurons could provide the basis for a spatiotopic hypothesis. For the second problem, saccadic suppression, visual masking and corollary discharge are well established mechanisms, and possible neuronal correlates have been identified for each.
4373687
The representation of visual salience in monkey parietal cortex
When natural scenes are viewed, a multitude of objects that are stable in their environments are brought in and out of view by eye movements. The posterior parietal cortex is crucial for the analysis of space, visual attention and movement. Neurons in one of its subdivisions, the lateral intraparietal area (LIP), have visual responses to stimuli appearing abruptly at particular retinal locations (their receptive fields). We have tested the responses of LIP neurons to stimuli that entered their receptive field by saccades. Neurons had little or no response to stimuli brought into their receptive field by saccades, unless the stimuli were behaviourally significant. We established behavioural significance in two ways: either by making a stable stimulus task-relevant, or by taking advantage of the attentional attraction of an abruptly appearing stimulus. Our results show that under ordinary circumstances the entire visual world is only weakly represented in LIP. The visual representation in LIP is sparse, with only the mostsalient or behaviourally relevant objects being strongly represented.
2795144
Remapping for visual stability
Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.
2819800
What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus.
Neuronal processing in cerebral cortex and signal transmission from cortex to brain stem have been studied extensively, but little is known about the numerous feedback pathways that ascend from brain stem to cortex. In this study, we characterized the signals conveyed through an ascending pathway coursing from the superior colliculus (SC) to the frontal eye field (FEF) via mediodorsal thalamus (MD). Using antidromic and orthodromic stimulation, we identified SC source neurons, MD relay neurons, and FEF recipient neurons of the pathway in Macaca mulatta. The monkeys performed oculomotor tasks, including delayed-saccade tasks, that permitted analysis of signals such as visual activity, delay activity, and presaccadic activity. We found that the SC sends all of these signals into the pathway with no output selectivity, i.e., the signals leaving the SC resembled those found generally within the SC. Visual activity arrived in FEF too late to contribute to short-latency visual responses there, and delay activity was largely filtered out in MD. Presaccadic activity, however, seemed critical because it traveled essentially unchanged from SC to FEF. Signal transmission in the pathway was fast ( approximately 2 ms from SC to FEF) and topographically organized (SC neurons drove MD and FEF neurons having similarly eccentric visual and movement fields). Our analysis of identified neurons in one pathway from brain stem to frontal cortex thus demonstrates that multiple signals are sent from SC to FEF with presaccadic activity being prominent. We hypothesize that a major signal conveyed by the pathway is corollary discharge information about the vector of impending saccades.
1892326
What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge.
One way we keep track of our movements is by monitoring corollary discharges or internal copies of movement commands. This study tested a hypothesis that the pathway from superior colliculus (SC) to mediodorsal thalamus (MD) to frontal eye field (FEF) carries a corollary discharge about saccades made into the contralateral visual field. We inactivated the MD relay node with muscimol in monkeys and measured corollary discharge deficits using a double-step task: two sequential saccades were made to the locations of briefly flashed targets. To make second saccades correctly, monkeys had to internally monitor their first saccades; therefore deficits in the corollary discharge representation of first saccades should disrupt second saccades. We found, first, that monkeys seemed to misjudge the amplitudes of their first saccades; this was revealed by systematic shifts in second saccade end points. Thus corollary discharge accuracy was impaired. Second, monkeys were less able to detect trial-by-trial variations in their first saccades; this was revealed by reduced compensatory changes in second saccade angles. Thus corollary discharge precision also was impaired. Both deficits occurred only when first saccades went into the contralateral visual field. Single-saccade generation was unaffected. Additional deficits occurred in reaction time and overall performance, but these were bilateral. We conclude that the SC-MD-FEF pathway conveys a corollary discharge used for coordinating sequential saccades and possibly for stabilizing vision across saccades. This pathway is the first elucidated in what may be a multilevel chain of corollary discharge circuits extending from the extraocular motoneurons up into cerebral cortex.
4395862
Influence of the thalamus on spatial visual processing in frontal cortex
Each of our movements activates our own sensory receptors, and therefore keeping track of self-movement is a necessary part of analysing sensory input. One way in which the brain keeps track of self-movement is by monitoring an internal copy, or corollary discharge, of motor commands. This concept could explain why we perceive a stable visual world despite our frequent quick, or saccadic, eye movements: corollary discharge about each saccade would permit the visual system to ignore saccade-induced visual changes. The critical missing link has been the connection between corollary discharge and visual processing. Here we show that such a link is formed by a corollary discharge from the thalamus that targets the frontal cortex. In the thalamus, neurons in the mediodorsal nucleus relay a corollary discharge of saccades from the midbrain superior colliculus to the cortical frontal eye field. In the frontal eye field, neurons use corollary discharge to shift their visual receptive fields spatially before saccades. We tested the hypothesis that these two components—a pathway for corollary discharge and neurons with shifting receptive fields—form a circuit in which the corollary discharge drives the shift. First we showed that the known spatial and temporal properties of the corollary discharge predict the dynamic changes in spatial visual processing of cortical neurons when saccades are made. Then we moved from this correlation to causation by isolating single cortical neurons and showing that their spatial visual processing is impaired when corollary discharge from the thalamus is interrupted. Thus the visual processing of frontal neurons is spatiotemporally matched with, and functionally dependent on, corollary discharge input from the thalamus. These experiments establish the first link between corollary discharge and visual processing, delineate a brain circuit that is well suited for mediating visual stability, and provide a framework for studying corollary discharge in other sensory systems.
8973933
Postsaccadic target blanking prevents saccadic suppression of image displacement
Displacement of a visual target during a saccadic eye movement is normally detected only at a high threshold, implying that high-quality information about target position is not stored in the nervous system across the saccade. We show that blanking the target for 50-300 msec after a saccade restores sensitivity to the displacement. With blanking, subjects reliably detect displacements as small as 0.33 deg across 6 deg eye movements, with correspondingly steep psychophysical functions. Performance with blanking in a fixation control is inferior, evidence for a saccadic enhancement of sensitivity to image displacement. If blanking is delayed so that the target is visible immediately after the saccade in its displaced position, performance declines to non-blanking levels. Blanking the target before the saccade, and restoring it during the saccade, yields a similar but weaker effect. We interpret these results with a model in which the visual system searches for the postsaccadic goal target within a restricted spatiotemporal window. If it is not found, the assumption of stationarity of the world is broken and the system makes use of other information such as extraretinal signals for calibrating location.
1300735
Immediate post-saccadic information mediates space constancy
We recently demonstrated that the perceived stability of a visual target that is displaced during a saccade critically depends on whether the target is present immediately when the saccade ends; blanking a target during and just after a saccade makes its intra-saccadic displacement more visible (Deubel et al. Vis Res 1996;36:985-996). Here, we investigate the interaction of visual context and blanking. Subjects saw a saccade target and an equal-sized distractor. During a saccade one or the other was displaced left or right. At the same time, one of the objects could be blanked briefly. Subjects reported whether the target or the distractor had jumped. The object that was blanked was more often seen as jumping (Experiment 1), regardless of which object really jumped, implying that continuously visible objects are preferentially perceived as stable. When both objects were blanked, longer blanking led to better accuracy at identifying which had jumped during a saccade. When one object was jumped and the other, stationary object was blanked (Experiment 2), the blanked object was mistakenly seen as jumping until the jump covered 50% or more of the saccade amplitude. In Experiment 3 a large continuously present texture underwent an undetected jump during a saccade, biasing judgments of simultaneous jumps of a blanked target. The results demonstrate that space constancy in normal situations is dominated by the assumption that a continuously present pattern is stable--this pattern becomes the spatial reference for the post-saccadic recalibration of perceptual space.
1903075
Transsaccadic memory of position and form.
Why and how people perceive the visual world as continuous and stable, despite the gross changes of its retinal projection that occur with each saccade, is one of the classic problems in perception. In the present paper, we argue that an important factor of visual stability and transsaccadic perception is formed by the reafferent visual information, i.e., the visual display that is present when the eyes land. After a review of some of the relevant theoretical, behavioural and physiological research on space constancy, saccadic suppression and transsaccadic memory, three experiments are presented. In a first experiment, we study the effect of an extended horizontal bar covering the target area for a short period after the saccade on saccadic suppression of image displacement. The results show that the bar acts just like a temporary blanking of the saccade target, leading to a strong reduction of saccadic suppression. In the second experiment, we show that any object that is present immediately after the saccade can establish a spatial reference, even if it is dissimilar to the saccade target. In a third experiment we study, with a similar approach, the effect of blanking and postsaccadic information on transsaccadic integration of form information. The data demonstrate that a localized postsaccadic object tends to replace the content of transsaccadic memory.
11541038
Failure to detect displacement of the visual world during saccadic eye movements
Abstract Perception of the rapid displacement of a target is suppressed during saccadic eye movements. Suppression is complete if eye movement is more than about three times larger than target displacement, and some suppression occurs even for target displacements of 4°. These results can be interpreted with the addition of a threshold element to the algebraic sum of the corollary discharge and the visual signal.
8620201
Post-saccadic location judgments reveal remapping of saccade targets to non-foveal locations.
The present study addresses the question of how objects are localized across saccades. In a task requiring participants to compare the location of a post-saccadic probe with the pre-saccadic target, we investigated the roles of saccade landing site and post-saccadic probe location. Saccade landing sites vary from trial to trial because of oculomotor error but can also be shifted by saccadic adaptation. Visual targets were extinguished during the saccade and reappeared after a short blank to counteract saccadic suppression of displacement. Performance in localizing targets after unadapted saccades was nearly veridical and independent of actual landing site, showing that trial-to-trial oculomotor error did not contribute to post-saccadic localization. This result suggests that much of the oculomotor error of saccades is included in the efference copy vector and this allows the recovery of a remapped target location that is often not foveal, but stable and accurate across trials. Displacement judgments relative to this remapped location will be independent of trial-to-trial variability in landing site. After adapted saccades, post-saccadic localization shifted in the direction opposite to adaptation but again, trial-by-trial landing site variability did not correlate with performance. This result suggests that the efference copy matches the planned upcoming saccade, be it adapted or not.
26922217
Human thalamus contributes to perceptual stability across eye movements
We continuously move our eyes when we inspect a visual scene. Although this leads to a rapid succession of discontinuous and fragmented retinal snapshots, we perceive the world as stable and coherent. Neural mechanisms underlying visual stability may depend on internal monitoring of planned or ongoing eye movements. In the macaque brain, a pathway for the transmission of such signals has been identified that is relayed by central thalamic nuclei. Here, we studied a possible role of this pathway for perceptual stability in a patient with a selective lesion affecting homologous regions of the human thalamus. Compared with controls, the patient exhibited a unilateral deficit in monitoring his eye movements. This deficit was manifest by a systematic inaccuracy both in successive eye movements and in judging the locations of visual stimuli. In addition, perceptual consequences of oculomotor targeting errors were erroneously attributed to external stimulus changes. These findings show that the human brain draws on transthalamic monitoring signals to bridge the perceptual discontinuities generated by our eye movements.
14618943
The proprioceptive representation of eye position in monkey primary somatosensory cortex
The cerebral cortex must have access to an eye position signal, as humans can report passive changes in eye position in total darkness, and visual responses in many cortical areas are modulated by eye position. The source of this signal is unknown. Here we demonstrate a representation of eye position in monkey primary somatosensory cortex, in the representation of the trigeminal nerve, near cells with a tactile representation of the contralateral brow. The neurons have eye position signals that increase monotonically with increasing orbital eccentricity from near the center of gaze, with directionally selectivity tuned in a Gaussian manner. All directions of eye position are represented in a single hemisphere. The signal is proprioceptive, because it can be obliterated by anesthetizing the contralateral orbit. It is not related to foveal or peripheral visual stimulation, and it represents the position of the eye in the head and not the angle of gaze in space.
60542175
Unix-based multiple-process system, for real-time data acquisition and control
Rex (real-time experimentation) is a real-time system that utilizes the multiple process structure of Unix to divide its functions among various cooperating processes. A running Rex system includes a comm process to control keyboard interaction, a scribe process to write data on disk, an int process to respond to interrupts from clocks, analog-to-digital converters, etc., and a display process to generate online graphic displays. A Rex system is not limited to these processes and may include others. This modular architecture is flexible and easy to maintain. Various applications may use the same comm and scribe but different ints or displays. The boundaries imposed by distributing Rex among multiple processes afford some protection against code becoming excessively intertwined and difficult to modify. Rex is written in c, a structured high level language. 7 references.
11112458
Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus.
The frontal eye field (FEF) and superior colliculus (SC) contribute to saccadic eye movement generation, and much of the FEF's oculomotor influence may be mediated through the SC. The present study examined the composition and topographic organization of signals flowing from FEF to SC by recording from FEF neurons that were antidromically activated from rostral or caudal SC. The first and most general result was that, in a sample of 88 corticotectal neurons, the types of signals relayed from FEF to SC were highly diverse, reflecting the general population of signals within FEF rather than any specific subset of signals. Second, many neurons projecting from FEF to SC carried signals thought to reflect cognitive operations, namely tonic discharges during the delay period of a delayed-saccade task (delay signals), elevated discharges during the gap period of a gap task (gap increase signals), or both. Third, FEF neurons discharging during fixation were found to project to the SC, although they did not project preferentially to rostral SC, where similar fixation neurons are found. Neurons that did project preferentially to the rostral SC were those with foveal visual responses and those pausing during the gap period of the gap task. Many of the latter neurons also had foveal visual responses, presaccadic pauses in activity, and postsaccadic increases in activity. These two types of rostral-projecting neurons therefore may contribute to the activity of rostral SC fixation neurons. Fourth, conduction velocity was used as an indicator of cell size to correct for sampling bias. The outcome of this correction procedure suggested that among the most prevalent neurons in the FEF corticotectal population are those carrying putative cognitive-related signals, i.e., delay and gap increase signals, and among the least prevalent are those carrying presaccadic burst discharges but lacking peripheral visual responses. Fifth, corticotectal neurons carrying various signals were biased topographically across the FEF. Neurons with peripheral visual responses but lacking presaccadic burst discharges were biased laterally, neurons with presaccadic burst discharges but lacking peripheral visual responses were biased medially, and neurons carrying delay or gap increase signals were biased dorsally. Finally, corticotectal neurons were distributed within the FEF as a function of their visual or movement field eccentricity and projected to the SC such that eccentricity maps in both structures were closely aligned. We conclude that the FEF most likely influences the activity of SC neurons continuously from the start of fixation, through visual analysis and cognitive manipulations, until a saccade is generated and fixation begins anew. Furthermore, the projection from FEF to SC is highly topographically organized in terms of function at both its source and its termination.
2535172
Frontal Eye Field Neurons Assess Visual Stability Across Saccades
The image on the retina may move because the eyes move, or because something in the visual scene moves. The brain is not fooled by this ambiguity. Even as we make saccades, we are able to detect whether visual objects remain stable or move. Here we test whether this ability to assess visual stability across saccades is present at the single-neuron level in the frontal eye field (FEF), an area that receives both visual input and information about imminent saccades. Our hypothesis was that neurons in the FEF report whether a visual stimulus remains stable or moves as a saccade is made. Monkeys made saccades in the presence of a visual stimulus outside of the receptive field. In some trials, the stimulus remained stable, but in other trials, it moved during the saccade. In every trial, the stimulus occupied the center of the receptive field after the saccade, thus evoking a reafferent visual response. We found that many FEF neurons signaled, in the strength and timing of their reafferent response, whether the stimulus had remained stable or moved. Reafferent responses were tuned for the amount of stimulus translation, and, in accordance with human psychophysics, tuning was better (more prevalent, stronger, and quicker) for stimuli that moved perpendicular, rather than parallel, to the saccade. Tuning was sometimes present as well for nonspatial transaccadic changes (in color, size, or both). Our results indicate that FEF neurons evaluate visual stability during saccades and may be general purpose detectors of transaccadic visual change.