Intervening Eye Movements Research Articles

Transsaccadic perceptual fusion.

Transsaccadic perceptual fusion is the integration of pre- and postsaccadic images into a single percept aligned in spatial coordinates. Several early studies reported an absence of transsaccadic fusion between dissimilar patterns, effectively stopping research on this question for three decades. We have now corrected two problematic aspects of these earlier studies and find robust evidence for transsaccadic perceptual fusion. First, we used simple pre- and postsaccadic targets, (|, ) for which spatial alignment is not critical. Second, we reduced the contrast of the postsaccadic stimulus, so that it would not suppress fusion. Participants reported seeing a superposition of the pre- and postsaccadic targets on 67% of trials. Importantly, we obtained similar results when the two stimuli were presented without an intervening eye movement, suggesting the existence of a general fusion mechanism. Directional biases in the saccade condition suggest that remapping might be the mechanism realigning the pre- and postsaccadic locations. Remapping may thus not only predict where targets will be located after a saccade but may also guide content, predicting what targets will look like. However, the constraints on the appearance of the fused percept suggest that it plays, at best, a limited role in visual stability across saccades.

A State Space Model for Spatial Updating of Remembered Visual Targets during Eye Movements.

In the oculomotor system, spatial updating is the ability to aim a saccade toward a remembered visual target position despite intervening eye movements. Although this has been the subject of extensive experimental investigation, there is still no unifying theoretical framework to explain the neural mechanism for this phenomenon, and how it influences visual signals in the brain. Here, we propose a unified state-space model (SSM) to account for the dynamics of spatial updating during two types of eye movement; saccades and smooth pursuit. Our proposed model is a non-linear SSM and implemented through a recurrent radial-basis-function neural network in a dual Extended Kalman filter (EKF) structure. The model parameters and internal states (remembered target position) are estimated sequentially using the EKF method. The proposed model replicates two fundamental experimental observations: continuous gaze-centered updating of visual memory-related activity during smooth pursuit, and predictive remapping of visual memory activity before and during saccades. Moreover, our model makes the new prediction that, when uncertainty of input signals is incorporated in the model, neural population activity and receptive fields expand just before and during saccades. These results suggest that visual remapping and motor updating are part of a common visuomotor mechanism, and that subjective perceptual constancy arises in part from training the visual system on motor tasks.

A Computational Model to Study the Dynamics of Updating of Remembered Visual Targets During Rapid and Slow Eye Movements

After an intervening eye movement, or saccade, humans and animals are able to localize previously perceived visual targets (spatial updating). Although efforts have been made to discover the mechanism underlying spatial updating, there are still many unanswered questions about the neuronal mechanism of this phenomenon. State space model is an effective method for modeling dynamical systems and it can represent the internal behaviour of these systems. Therefore, we developed a state space model for updating target-related spatial information in gaze-centered coordinates. We considered three types of input in our proposed model: 1) an efference copy signal, inspired by motor burst in SC, 2) an eye position signal, found in LIP, VIP, MT and MST areas and 3) visual topographic maps of visual stimuli, located in SC. To model the internal neuronal behaviour of the system, we developed a radial basis function neural network (RBFNN) which can be trained with an Extended Kalman filter method. This RBFNN represents the state space and we can obtain a topographic map of the remembered target in its hidden layer. From our proposed model, the output obtained is the decoded location of the remembered target. To explore the internal mechanism underlying the updating process, we trained this model on a double-step saccade-saccade or pursuit-saccade task. After training, the receptive fields of state-space units replicated both predictive remapping during saccades (Duhamel et al. Science 1992) and continuous eye-centered updating during smooth pursuit (Dash et al. Current Biology, in press). In addition, during trans-saccadic remapping, receptive fields also expanded (to our knowledge, this predicted expansion has not yet been reported in the published literature). In the future, we plan to incorporate this framework within a more comprehensive model of trans-saccadic integration of both spatial and feature information, and use this framework to construct a physiologically plausible model. Meeting abstract presented at VSS 2015. Language: en

Target-distractor competition in the oculomotor system is spatiotopic.

In natural scenes, multiple visual stimuli compete for selection; however, each saccade displaces the stimulus representations in retinotopicaly organized visual and oculomotor maps. In the present study, we used saccade curvature to investigate whether oculomotor competition across eye movements is represented in retinotopic or spatiotopic coordinates. Participants performed a sequence of saccades and we induced oculomotor competition by briefly presenting a task-irrelevant distractor at different times during the saccade sequence. Despite the intervening saccade, the second saccade curved away from a spatial representation of the distractor that was presented before the first saccade. Furthermore, the degree of saccade curvature increased with the salience of the distractor presented before the first saccade. The results suggest that spatiotopic representations of target-distractor competition are crucial for successful interaction with objects of interest despite the intervening eye movements.

Eye position information is used to compensate the consequences of ocular torsion on V1 receptive fields

It is commonly held that the receptive fields (RFs) of neurons in primary visual cortex (V1) are fixed relative to the retina. Hence, V1 should be unable to distinguish between retinal image shifts due to object motion and image shifts resulting from ego motion. Here we show that, in contrast to this belief, a particular class of neurons in V1 of non-human primates have RFs that are actually head centred, despite intervening eye movements. They use eye position information to shift their RFs location and to change their orientation tuning on the retina so as to fully compensate for the retinal consequences of a particular type of reflexive eye movements, ocular counter-roll, an eye rotation around the line of sight partially counterpoising head tilt. In other words, V1 uses eye position information to resolve the ambiguity if retinal image tilt is the result of the tilting of an object or of the ocular counter-roll.

Allocentrically implied target locations are updated in an eye-centred reference frame

When reaching to remembered target locations following an intervening eye movement a systematic pattern of error is found indicating eye-centred updating of visuospatial memory. Here we investigated if implicit targets, defined only by allocentric visual cues, are also updated in an eye-centred reference frame as explicit targets are. Participants viewed vertical bars separated by varying distances, and horizontal lines of equivalently varying lengths, implying a “target” location at the midpoint of the stimulus. After determining the implied “target” location from only the allocentric stimuli provided, participants saccaded to an eccentric location, and reached to the remembered “target” location. Irrespective of the type of stimulus reaching errors to these implicit targets are gaze-dependent, and do not differ from those found when reaching to remembered explicit targets. Implicit target locations are coded and updated as a function of relative gaze direction with respect to those implied locations just as explicit targets are, even though no target is specifically represented.

Dissociation between intentional and automatic remapping: Different levels of inter-hemispheric transfer

In order to efficiently interact with our environment we need to constantly to update the spatial representation of visual targets for movement. This is required not only when we move our eyes but also when we want to reach toward a location different from the actual physical target (for example symmetrical). These two types of remapping are very different in nature, one being automatic, and the other intentional. However, they both have been shown to involve the posterior parietal cortex (PPC). To further investigate the role of this brain region in automatic and intentional remapping processes and the level of inter-hemispheric transfer of visuo-motor information in these two conditions of reaching, we tested two patients with unilateral optic ataxia (OA) in two different tasks: reaching to a memorised visual target after an intervening eye movement (trans-saccadic remapping) and an anti-reaching task. We showed that lesions of the PPC had different implications for these two tasks. In the trans-saccadic remapping task, movements toward the contralesional field were disrupted, even when the visual target was presented in the ipsilesional field. In contrast, in the anti-reaching task, the patients were mostly impaired in conditions where the target was presented in the contralesional field, even if the movement was executed toward the ipsilesional field. We postulate that the transfer of the visuo-motor information between hemispheres occurs before the parietal cortex in trans-saccadic remapping (transfer of visual information), and at the parietal level or after in anti-reaching (transfer of visuo-motor information).

Spatiotopic apparent motion reveals local variations in space constancy

While participants made 10° horizontal saccades, two dots were presented, one before and one after the saccade. Each dot was presented for 400 ms, the first turned off about 100 ms before, while the second turned on about 100 ms after the saccade. The two dots were separated vertically by 3°, but because of the intervening eye movement, they were also separated horizontally on the retina by an additional 10°. Participants nevertheless reported that the perceived motion was much more vertical than horizontal, suggesting that the trans-saccadic displacement was corrected, at least to some extent, for the retinal displacement caused by the eye movement. The corrections were not exact, however, showing significant biases that corresponded to about 5% of the saccade amplitude. The perceived motion between the probes was tested at 9 different locations and the biases, the deviations from accurate correction, varied significantly across locations. Two control experiments for judgments of position and of verticality of motion without eye movement confirmed that these biases are specific to the correction for the saccade. The local variations in the correction for saccades are consistent with physiological "remapping" proposals for space constancy that individually correct only a few attended targets but are not consistent with global mechanisms that predict the same correction at all locations.

Saccadic updating of object orientation for grasping movements

Reach and grasp movements are a fundamental part of our daily interactions with the environment. This spatially-guided behavior is often directed to memorized objects because of intervening eye movements that caused them to disappear from sight. How does the brain store and maintain the spatial representations of objects for future reach and grasp movements? We had subjects ( n = 8) make reach and two-digit grasp movements to memorized objects, briefly presented before an intervening saccade. Grasp errors, characterizing the spatial representation of object orientation, depended on current gaze position, with and without intervening saccade. This suggests that the orientation information of the object is coded and updated relative to gaze during intervening saccades, and that the grasp errors arose after the updating stage, during the later transformations involved in grasping. The pattern of reach errors also revealed a gaze-centered updating of object location, consistent with previous literature on updating of single-point targets. Furthermore, grasp and reach errors correlated strongly, but their relationship had a non-unity slope, which may suggest that the gaze-centered spatial updates were made in separate channels. Finally, the errors of the two digits were strongly correlated, supporting the notion that these were not controlled independently to form the grip in these experimental conditions. Taken together, our results suggest that the visuomotor system dynamically represents the short-term memory of location and orientation information for reach-and-grasp movements.

Locations of serial reach targets are coded in multiple reference frames

Previous work from our lab, and elsewhere, has demonstrated that remembered target locations are stored and updated in an eye-fixed reference frame. That is, reach errors systematically vary as a function of gaze direction relative to a remembered target location, not only when the target is viewed in the periphery ( Bock, 1986, known as the retinal magnification effect), but also when the target has been foveated, and the eyes subsequently move after the target has disappeared but prior to reaching (e.g., Henriques, Klier, Smith, Lowy, & Crawford, 1998; Sorrento & Henriques, 2008; Thompson & Henriques, 2008). These gaze-dependent errors, following intervening eye movements, cannot be explained by representations whose frame is fixed to the head, body or even the world. However, it is unknown whether targets presented sequentially would all be coded relative to gaze (i.e., egocentrically/absolutely), or if they would be coded relative to the previous target (i.e., allocentrically/relatively). It might be expected that the reaching movements to two targets separated by 5° would differ by that distance. But, if gaze were to shift between the first and second reaches, would the movement amplitude between the targets differ? If the target locations are coded allocentrically (i.e., the location of the second target coded relative to the first) then the movement amplitude should be about 5°. But, if the second target is coded egocentrically (i.e., relative to current gaze direction), then the reaches to this target and the distances between the subsequent movements should vary systematically with gaze as described above. We found that requiring an intervening saccade to the opposite side of 2 briefly presented targets between reaches to them resulted in a pattern of reaching error that systematically varied as a function of the distance between current gaze and target, and led to a systematic change in the distance between the sequential reach endpoints as predicted by an egocentric frame anchored to the eye. However, the amount of change in this distance was smaller than predicted by a pure eye-fixed representation, suggesting that relative positions of the targets or allocentric coding was also used in sequential reach planning. The spatial coding and updating of sequential reach target locations seems to rely on a combined weighting of multiple reference frames, with one of them centered on the eye.

A deficit of spatial remapping in constructional apraxia after right-hemisphere stroke

Constructional apraxia refers to the inability of patients to copy accurately drawings or three-dimensional constructions. It is a common disorder after right parietal stroke, often persisting after initial problems such as visuospatial neglect have resolved. However, there has been very little experimental investigation regarding mechanisms that might contribute to the syndrome. Here, we examined whether a key deficit might be failure to integrate visual information correctly from one fixation to the next. Specifically, we tested whether this deficit might concern remapping of spatial locations across saccades. Right-hemisphere stroke patients with constructional apraxia were compared to patients without constructional problems and neurologically healthy controls. Participants judged whether a pattern shifted position (spatial task) or changed in pattern (non-spatial task) across two saccades, compared to a control condition with an equivalent delay but without intervening eye movements. Patients with constructional apraxia were found to be significantly impaired in position judgements with intervening saccades, particularly when the first saccade of the sequence was to the right. The importance of these remapping deficits in constructional apraxia was confirmed through a highly significant correlation between saccade task performance and constructional impairment on standard neuropsychological tasks. A second study revealed that even single saccades to the right can impair constructional apraxia patients' perception of location shifts. These data are consistent with the view that rightward eye movements result in loss of remembered spatial information from previous fixations, presumably due to constructional apraxia patients' damage to the right-hemisphere regions involved in remapping locations across saccades. These findings provide the first evidence for a deficit in remapping visual information across saccades underlying right-hemisphere constructional apraxia.

Visual Remapping by Vector Subtraction: Analysis of Multiplicative Gain Field Models

Saccadic eye movements remain spatially accurate even when the target becomes invisible and the initial eye position is perturbed. The brain accomplishes this in part by remapping the remembered target location in retinal coordinates. The computation that underlies this visual remapping is approximated by vector subtraction: the original saccade vector is updated by subtracting the vector corresponding to the intervening eye movement. The neural mechanism by which vector subtraction is implemented is not fully understood. Here, we investigate vector subtraction within a framework in which eye position and retinal target position signals interact multiplicatively (gain field). When the eyes move, they induce a spatial modulation of the firing rates across a retinotopic map of neurons. The updated saccade metric can be read from the shift of the peak of the population activity across the map. This model uses a quasi-linear (half-rectified) dependence on the eye position and requires the slope of the eye position input to be negatively proportional to the preferred retinal position of each neuron. We derive analytically this constraint and study its range of validity. We discuss how this mechanism relates to experimental results reported in the frontal eye fields of macaque monkeys.

Judging relative positions across saccades

When components of a shape are presented asynchronously during smooth pursuit, the retinal image determines the perceived shape, as if the parts belong to the moving object that the eyes are pursuing. Saccades normally shift our gaze between structures of interest, so there is no reason to expect anything to have moved with the eyes. We therefore decided to examine how people judge the separation between a target flashed before and another flashed after a saccade. Subjects tracked a jumping dot with their eyes. Targets were flashed at predetermined retinal positions, with a 67–242 ms interval between the flashes. After each trial subjects indicated where they had seen the targets. We selected the trials on which subjects made a complete saccade between the presentations of the two targets. For short inter-target intervals, subjects’ judgements depended almost exclusively on the retinal separation, even when there were conspicuous visual references nearby. Even for the longest intervals, only part of the change in eye orientation was taken into consideration. These findings cannot simply be accounted for on the basis of the mislocalisation of individual targets or a compression of space near saccades. We conclude that the retinal separation determines the perceived separation between targets presented with a short interval between them, irrespective of any intervening eye movements.

Visuospatial updating of reaching targets in near and far space.

The brain constructs multiple representations of near and far space but it is unclear which spatial mechanism guides reaching across eye movements in near space. Retinocentric reaching representations are known to exist in parietal cortex, but must be updated during eye movements, in order to remain accurate. In contrast, non-retinal (e.g. muscle-centered) reaching plans in motor cortex do not require updating, and so may provide a more stable encoding mechanism. To test between these, we employed a behavioral test. Subjects briefly foveated a target (located at various depths in near and far space) looked peripherally, then reached toward its remembered location. Surprisingly, subjects did not use the stable non-retinal reaching plan (compared to controls without eye movements). Instead, the intervening eye movements induced a systematic pattern of reaching errors for targets at all depths consistent with updating in a retinal frame. We conclude that a common eye-centered updating mechanism prevails in programming arm movements in both near and far space.

Body-centered representations for visually-guided action emerge during early infancy

The nature of the spatial representations that underlie simple visually guided actions early in life were investigated through the application of a `double-step' saccade paradigm to 3- and 7-month-old infants. Saccades in the older infants, like those observed in adults, were executed within body-centered spatial coordinates that take into account the effects of intervening eye movements. In contrast, younger infants tended to respond according to the targets' retinocentric locations and did not incorporate the effects of displacements caused by previous saccades. These results indicate that, contrary to prevailing views, body-centered representations for action are not present from birth but emerge, probably through experience, over the first few months of life.

Measuring the effect of multiple eye fixations on memory for visual attributes.

Because of limited peripheral vision, many visual tasks depend on multiple eye fixations. Good performance in such tasks demonstrates that some memory must survive from one fixation to the next. One factor that must influence performance is the degree to which multiple eye fixations interfere with the critical memories. In the present study, the amount of interference was measured by comparing visual discriminations based on multiple fixations to visual discriminations based on a single fixation. The procedure resembled partial report, but used a discrimination measure. In the prototype study, two lines were presented, followed by a single line and a cue. The cue pointed toward one of the positions of the first two lines. Observers were required to judge if the single line in the second display was longer or shorter than the cued line of the first display. These judgments were used to estimate a length threshold. The critical manipulation was to instruct observers either to maintain fixation between the lines of the first display or to fixate each line in sequence. The results showed an advantage for multiple fixations despite the intervening eye movements. In fact, thresholds for the multiple-fixation condition were nearly as good as those in a control condition where the lines were foveally viewed without eye movements. Thus, eye movements had little or no interfering effect in this task. Additional studies generalized the procedure and the stimuli. In conclusion, information about a variety of size and shape attributes was remembered with essentially no interference across eye fixations.

Eye position signals in human saccadic processing.

1. We studied saccades to briefly flashed targets in 8 human subjects. The target flash occurred (i) during smooth pursuit ("ramp-flash"), (ii) just before a saccade to another target ("step-flash"), or (iii) during steady fixation ("flash only"). All lights were extinguished after the target flash so that smooth pursuit or saccadic eye movements occurred during the interval of complete darkness between the target flash and the saccade to it. We compared these saccades to those made without intervening eye movement (flash only), and quantified the extent to which the saccadic system compensated for the change in eye position that occurred during the dark interval. 2. Saccades to control flashes were reasonably accurate (mean gain 0.87) and consistent. Compensation for the intervening eye movement in the ramp-flash and step-flash paradigms was highly variable from trial to trial. On average, subjects compensated for 27% of the intervening pursuit eye movement on ramp-flash trials and for 58% of intervening saccadic movement on step-flash trials. 3. Multiple regression analysis showed that the variability did not depend on factors such as variations in underlying saccadic gain, response latency, timing of stimuli or size of the required response. We conclude that this variability is intrinsic to saccadic responses that require the use of an eye position signal. 4. These results show that an eye position signal is available to the saccadic system but that this signal has low fidelity.(ABSTRACT TRUNCATED AT 250 WORDS)

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.