Sequences Of Saccades Research Articles

Trajectory curvature in saccade sequences: spatiotopic influences vs. residual motor activity.

When decisions drive saccadic eye movements, traces of the decision process can be inferred from the movement trajectories. For example, saccades can curve away from distractor stimuli, which was thought to reflect cortical inhibition biasing activity in the superior colliculus. Recent neurophysiological work does not support this theory, and two recent models have replaced top-down inhibition with lateral interactions in the superior colliculus or neural fatigue in the brainstem saccadic burst generator. All current models operate in retinotopic coordinates and are based on single saccade paradigms. To extend these models to sequences of saccades, we assessed whether and how saccade curvature depends on previously fixated locations and the direction of previous saccades. With a two-saccade paradigm, we first demonstrated that second saccades curved away from the initial fixation stimulus. Furthermore, by varying the time from fixation offset and the intersaccadic duration, we distinguished the extent of curvature originating from the spatiotopic representation of the previous fixation location or residual motor activity of the previous saccade. Results suggest that both factors drive curvature, and we discuss how these effects could be implemented in current models. In particular, we propose that the collicular retinotopic maps receive an excitatory spatiotopic update from the lateral interparial region.NEW & NOTEWORTHY Saccades curve away from locations of previous fixation. Varying stimulus timing demonstrates the effects of both 1) spatiotopic representation and 2) motor residual activity from previous saccades. The spatiotopic effect can be explained if current models are augmented with an excitatory top-down spatiotopic signal.

Predictive and tempo-flexible synchronization to a visual metronome in monkeys

Predictive and tempo-flexible synchronization to an auditory beat is a fundamental component of human music. To date, only certain vocal learning species show this behaviour spontaneously. Prior research training macaques (vocal non-learners) to tap to an auditory or visual metronome found their movements to be largely reactive, not predictive. Does this reflect the lack of capacity for predictive synchronization in monkeys, or lack of motivation to exhibit this behaviour? To discriminate these possibilities, we trained monkeys to make synchronized eye movements to a visual metronome. We found that monkeys could generate predictive saccades synchronized to periodic visual stimuli when an immediate reward was given for every predictive movement. This behaviour generalized to novel tempi, and the monkeys could maintain the tempo internally. Furthermore, monkeys could flexibly switch from predictive to reactive saccades when a reward was given for each reactive response. In contrast, when humans were asked to make a sequence of reactive saccades to a visual metronome, they often unintentionally generated predictive movements. These results suggest that even vocal non-learners may have the capacity for predictive and tempo-flexible synchronization to a beat, but that only certain vocal learning species are intrinsically motivated to do it.

Switch from ambient to focal processing mode explains the dynamics of free viewing eye movements

Previous studies have reported that humans employ ambient and focal modes of visual exploration while they freely view natural scenes. These two modes have been characterized based on eye movement parameters such as saccade amplitude and fixation duration, but not by any visual features of the viewed scenes. Here we propose a new characterization of eye movements during free viewing based on how eyes are moved from and to objects in a visual scene. We applied this characterization to data obtained from freely-viewing macaque monkeys. We show that the analysis based on this characterization gives a direct indication of a behavioral shift from ambient to focal processing mode along the course of free viewing exploration. We further propose a stochastic model of saccade sequence generation incorporating a switch between the two processing modes, which quantitatively reproduces the behavioral features observed in the data.

Saccade Sequences and Rapid Number Naming in Chronic Concussion (P6.040)

Saccade Sequences and Rapid Number Naming in Chronic Concussion (P6.040)

Interaction between the oculomotor and postural systems during a dual-task: Compensatory reductions in head sway following visually-induced postural perturbations promote the production of accurate double-step saccades in standing human adults.

Humans routinely scan their environment for useful information using saccadic eye movements and/or coordinated movements of the eyes and other body segments such the head and the torso. Most previous eye movement studies were conducted with seated subject and showed that single saccades and sequences of saccades (e.g. double-step saccades) made to briefly flashed stimuli were equally accurate and precise. As one can easily appreciate, most gaze shifts performed daily by a given person are not produced from a seated position, but rather from a standing position either as subjects perform an action from an upright stance or as they walk from one place to another. In the experiments presented here, we developed a new dual-task paradigm in order to study the interaction between the gaze control system and the postural system. Healthy adults (n = 12) were required to both maintain balance and produce accurate single-step and double-step eye saccades from a standing position. Visually-induced changes in head sway were evoked using wide-field background stimuli that either moved in the mediolateral direction or in the anteroposterior direction. We found that, as in the seated condition, single- and double-step saccades were very precise and accurate when made from a standing position, but that a tighter control of head sway was necessary in the more complex double-step saccades condition for equivalent results to be obtained. Our perturbation results support the “common goal” hypothesis that state that if necessary, as was the case during the more complex oculomotor task, context-dependent modulations of the postural system can be triggered to reduced instability and therefore support the accomplishment of a suprapostural goal.

Parallel activation of prospective motor plans during visually-guided sequential saccades.

Behavioural evidences suggest that sequential saccades to multiple stimuli are planned in parallel. However, it remains unclear whether such parallel programming reflects concurrent processing of goals or whether multiple motor plans coexist, unfolding subsequently during execution. Here we use midway saccades, directed at intermediate locations between two targets, as a probe to address this question in a novel double-step adaptation task. The task consisted of trials where subjects had to follow the appearance of two targets presented in succession with two sequential saccades. In some trials, the second target predictably jumped to a new location during the second saccade. Initially, the second saccade was aimed at the final target's location before the jump. As subjects adapted to the target jump, saccades were aimed to the second target's new location. We tested whether the spatial distribution of midway saccades could be explained as an interaction between two concurrent saccade goals, each directed at the two target locations, or between the initial motor plan to the first target location and a prospective motor plan directed from the initial to the final target location. A shift in the midway saccades' distribution towards the jumped location of the second target following adaptation indicated that the brain can make use of prospective motor plans to guide sequential eye movements. Furthermore, we observed that the spatiotemporal pattern of endpoints of midway saccades can be well explained by a motor addition model. These results provide strong evidence of parallel activation of prospective motor plans during sequential saccades.

The Concurrent Programming of Saccades.

Sequences of saccades have been shown to be prepared concurrently however it remains unclear exactly what aspects of those saccades are programmed in parallel. To examine this participants were asked to make one or two target-driven saccades: a reflexive saccade; a voluntary saccade; a reflexive then a voluntary saccade; or vice versa. During the first response the position of a second target was manipulated. The new location of the second saccade target was found to impact on second saccade latencies and second saccade accuracy showing that some aspects of the second saccade program are prepared in parallel with the first. However, differences were found in the specific pattern of effects for each sequence type. These differences fit well within a general framework for saccade control in which a common priority map for saccade control is computed and the influence of saccade programs on one another depends not so much on the types of saccade being produced but rather on the rate at which their programs develop.

Contributions of gaze-centered and object-centered coding in a double-step saccade task.

The position of a saccade target can be encoded in gaze-centered coordinates, that is, relative to the current gaze position, or in object-centered coordinates, that is, relative to an object in the environment. We tested the role of gaze-centered and object-centered coding in a double-step saccade task involving the Brentano version of the Müller-Lyer illusion. The two visual targets were presented either sequentially, requiring gaze-centered coding of the second saccade target, or simultaneously, thereby providing additional object-centered information about the location of the second target relative to the first. We found that the endpoint of the second saccade was affected by the illusion, irrespective of whether the targets were presented sequentially or simultaneously, suggesting that participants used a gaze-centered updating strategy. We found that variability in saccade endpoints was reduced when object-centered information was consistently available but not when its presence varied from trial to trial. Our results suggest that gaze-centered coding is dominant in the planning of sequential saccades, whereas object-centered information plays a relatively small role.

Error compensation in random vector double step saccades with and without global adaptation

In saccade sequences without visual feedback endpoint errors pose a problem for subsequent saccades. Accurate error compensation has previously been demonstrated in double step saccades (DSS) and is thought to rely on a copy of the saccade motor vector. However, these studies typically use fixed target vectors on each trial, calling into question the generalizability of the findings due to the high stimulus predictability.We present a random walk DSS paradigm (random target vector amplitudes and directions) to provide a more complete, realistic and generalizable description of error compensation in saccade sequences. We regressed the vector between the endpoint of the second saccade and the endpoint of a hypothetical second saccade that does not take first saccade error into account on the ideal compensation vector. This provides a direct and complete estimation of error compensation in DSS. We observed error compensation with varying stimulus displays that was comparable to previous findings. We also employed this paradigm to extend experiments that showed accurate compensation for systematic undershoots after specific-vector saccade adaptation. Utilizing the random walk paradigm for saccade adaptation by Rolfs et al. (2010) together with our random walk DSS paradigm we now also demonstrate transfer of adaptation from reactive to memory guided saccades for global saccade adaptation.We developed a new, generalizable DSS paradigm with unpredictable stimuli and successfully employed it to verify, replicate and extend previous findings, demonstrating that endpoint errors are compensated for saccades in all directions and variable amplitudes.

Contextual saccade adaptation as a tool to investigate sequential saccades.

Saccade adaptation can be contextual; meaning that saccade gain for the same retinotopic target location can differ depending on the context. In this study we used reflexive and sequential scanning saccades as contexts in order to investigate whether saccadic sequences are processed differently from single saccades. In Experiment 1, subjects were instructed to perform either a single downward-vertical saccade when the initial fixation point was presented at the center of the monitor (reflexive trials), or a sequence of two saccades when the fixation point was located on the right side of the monitor (scanning trials), where the second saccade of the scanning trials was the same as the saccades in the reflexive trials. The scanning and reflexive trials were interleaved. After a baseline phase, in the adapting phase, we induced opposite saccadic adaptation (gain-increasing and gain-decreasing) in the reflexive and scanning trials using a double-step procedure. The experiment terminated with a post-adapting phase, similar to the baseline. Results showed a gradual saccadic gain change, in opposite directions, for scanning and reflexive trials. The reflexive and scanning saccadic amplitudes at the end of the adapting phase and even in the post-adapting phase were significantly different, indicating strong contextual saccade adaptation. Experiment 2 was similar to Experiment 1, except that we replaced the reflexive trials with sequential saccades from the left-side of the monitor and tried to induce contextual saccade adaptation in the second saccade of the two different saccade sequences. Surprisingly, we did not find any significant shifts in saccadic gain in Experiment 2. The fact that saccades in the reflexive and scanning contexts can be adapted independently provides evidence that these two types of saccades are planned and performed differently. However scanning saccades from two different sequences cannot be adapted in opposite directions, suggesting that adaptation is transferred between them. Meeting abstract presented at VSS 2016

Adaptation of Saccadic Sequences with and without Remapping.

It is relatively easy to adapt visually-guided saccades because the visual vector and the saccade vector match. The retinal error at the saccade landing position is compared to the prediction error, based on target location and efference copy. If these errors do not match, planning processes at the level(s) of the visual and/or motor vector processing are assumed to be inaccurate and the saccadic response is adjusted. In the case of a sequence of two saccades, the final error can be attributed to the last saccade vector or to the entire saccadic displacement. Here, we asked whether and how adaptation can occur in the case of remapped saccades, such as during the classic double-step saccade paradigm, where the visual and motor vectors of the second saccade do not coincide and so the attribution of error is ambiguous. Participants performed saccades sequences to two targets briefly presented prior to first saccade onset. The second saccade target was either briefly re-illuminated (sequential visually-guided task) or not (remapping task) upon first saccade offset. To drive adaptation, the second target was presented at a displaced location (backward or forward jump condition or control—no jump) at the end of the second saccade. Pre- and post-adaptation trials were identical, without the re-appearance of the target after the second saccade. For the 1st saccade endpoints, there was no change as a function of adaptation. For the 2nd saccade, there was a similar increase in gain in the forward jump condition (52% and 61% of target jump) in the two tasks, whereas the gain decrease in the backward condition was much smaller for the remapping task than for the sequential visually-guided task (41% vs. 94%). In other words, the absolute gain change was similar between backward and forward adaptation for remapped saccades. In conclusion, we show that remapped saccades can be adapted, suggesting that the error is attributed to the visuo-motor transformation of the remapped visual vector. The mechanisms by which adaptation takes place for remapped saccades may be similar to those of forward sequential visually-guided saccades, unlike those involved in adaptation for backward sequential visually-guided saccades.

Voluntary eye movements direct attention on the mental number space.

Growing evidence suggests that orienting visual attention in space can influence the processing of numerical magnitude, with leftward orienting speeding up the processing of small numbers relative to larger ones and the converse for rightward orienting. The manipulation of eye movements is a convenient way to direct visuospatial attention, but several aspects of the complex relationship between eye movements, attention orienting and number processing remain unexplored. In a previous study, we observed that inducing involuntary, reflexive eye movements by means of optokinetic stimulation affected number processing only when numerical magnitude was task relevant (i.e., during magnitude comparison, but not during parity judgment; Ranzini et al., in J Cogn Psychol 27, 459-470, (2015). Here, we investigated whether processing of task-irrelevant numerical magnitude can be modulated by voluntary eye movements, and whether the type of eye movements (smooth pursuit vs. saccades) would influence this interaction. Participants tracked with their gaze a dot while listening to a digit. The numerical task was to indicate whether the digit was odd or even through non-spatial, verbal responses. The dot could move leftward or rightward either continuously, allowing tracking by smooth pursuit eye movements, or in discrete steps across a series of adjacent locations, triggering a sequence of saccades. Both smooth pursuit and saccadic eye movements similarly affected number processing and modulated response times for large numbers as a function of direction of motion. These findings suggest that voluntary eye movements redirect attention in mental number space and highlight that eye movements should play a key factor in the investigation of number-space interactions.

Probing the dynamics of perisaccadic vision with EEG

Eye movements (saccades) are a necessary component of vision – with a sequence of saccades, we can explore the entire visual scene quickly. The role of saccades is beyond mechanical, in fact they are closely tied to mechanisms of visual cognition, in particular to spatial attention. Two physiological processes, pre-saccadic shifts of attention and saccadic suppression illustrate the interplay of saccades and visual perception: while the attentional shift enhances visual sensitivity to the future saccade target, saccadic suppression inhibits it for non-target objects. Both processes are transient and active already before the saccade onset. So far, these processes have been studied primarily behaviorally in human subjects or via invasive electrophysiological recordings in monkeys. Despite considerable advances, a physiological characterization of these two mechanisms is still lacking in the human literature. Here, we will present a new methodology for investigating perisaccadic events in human subjects. Using electroencephalography (EEG) co-registered with eye tracking (ET), we sampled the complete time-course of perisaccadic activity and identified two ERP components – pre-saccadic voltage enhancement and post-saccadic voltage reduction – that likely relate to shifts of spatial attention and saccadic suppression.

Visual mislocalization during double-step saccades.

Visual objects presented briefly at the time of saccade onset appear compressed toward the saccade target. Compression strength depends on the presentation of a visual saccade target signal and is strongly reduced during the second saccade of a double-step saccade sequence (Zimmermann et al., 2014b). Here, I tested whether perisaccadic compression is linked to saccade planning by contrasting two double-step paradigms. In the same-direction double-step paradigm, subjects were required to perform two rightward 10° saccades successively. At various times around execution of the saccade sequence a probe dot was briefly flashed. Subjects had to localize the position of the probe dot after they had completed both saccades. I found compression of visual space only at the time of the first but not at the time of the second saccade. In the reverse-direction paradigm, subjects performed first a rightward 10° saccade followed by a leftward 10° saccade back to initial fixation. In this paradigm compression was found in similar magnitude during both saccades. Analysis of the saccade parameters did not reveal indications of saccade sequence preplanning in this paradigm. I therefore conclude that saccade planning, rather than saccade execution factors, is involved in perisaccadic compression.

Spatial gradients of oculomotor inhibition of return in deaf and normal adults.

We explored the effect of deafness on the spatial (gradient) and temporal (decay) properties of oculomotor inhibition of return (IOR) using a task developed by Vaughan (Theoretical and applied aspects of eye movement research. Elsevier, North Holland, pp 143-150, 1984) in which participants made a sequence of saccades to carefully placed targets . Unlike IOR tasks in which ignored cues are used to explore the aftereffects of covert orienting, this task better approximates real-world behavior in which participants are free to make eye movements to potentially relevant inputs. Because IOR is a bias against returning attention and gaze to a previously attended location, we expected to find, and we did find, slower saccades toward previously fixated locations. Replicating Vaughan, a gradient of inhibition around a previously fixated location was observed and this inhibition began to decay after 1200 ms. Importantly, there were no significant differences between the deaf and the normal hearing subjects, on neither the magnitude of oculomotor IOR, nor its decay over time, nor its gradient around the previously fixated location .

For your eyes only [eye-tracking video gaming

Can eye-tracking technology move beyond niche applications and into the mainstream - and would you want it to?. Eye tracking has been around for decades, used by researchers studying the physiology and psychology of human vision. But with rapidly falling costs and recent technological advances, the tech is finally moving away from passive analysis and into the area of active interaction. People with disabilities use it to move the cursor on a computer screen, and there are trials to get them to control their prosthetic limbs just by using their gaze. Eye-tracking video gaming isstarting to take off, and many firms are beginning to explore the tech to understand how their customers react to adverts and shop displays using state-of-the-art headsets with integrated eye tracking. In the following decades this approach flourished, with a host of techniques that relied on recording reflections from light bouncing off the eye. Specifically, academics looked at how tracking the eye's endless sequence of fixations (pauses on a specific area) and saccades (rapid movementsbetween fixations) could help them better understand the visual system and even spot neurological disorders; as computers became widely available, they could even compute and analyse subtle differences in gaze patterns that are not noticed by humans.

Abnormal non nystagmic spontaneous eye movements

SummaryWhen the saccadic system is dysfunctional, an intrusion of spontaneous unwanted saccades can disrupt visual fixation. These can present as square wave jerks, ocular flutter and opsoclonus. Voluntary nystagmus is also a sequence of abnormal saccades. At the end of the session, participants should be able to identify these specific eye movement disorders and organize proper investigations accordingly.

Corollary Discharge Failure in an Oculomotor Task Is Related to Delusional Ideation in Healthy Individuals.

Predicting the sensory consequences of saccadic eye movements likely plays a crucial role in planning sequences of saccades and in maintaining visual stability despite saccade-caused retinal displacements. Deficits in predictive activity, such as that afforded by a corollary discharge signal, have been reported in patients with schizophrenia, and may lead to the emergence of positive symptoms, in particular delusions of control and auditory hallucinations. We examined whether a measure of delusional thinking in the general, non-clinical population correlated with measures of predictive activity in two oculomotor tasks. The double-step task measured predictive activity in motor control, and the in-flight displacement task measured predictive activity in trans-saccadic visual perception. Forty-one healthy adults performed both tasks and completed a questionnaire to assess delusional thinking. The quantitative measure of predictive activity we obtained correlated with the tendency towards delusional ideation, but only for the motor task, and not the perceptual task: Individuals with higher levels of delusional thinking showed less self-movement information use in the motor task. Variation of the degree of self-generated movement knowledge as a function of the prevalence of delusional ideation in the normal population strongly supports the idea that corollary discharge deficits measured in schizophrenic patients in previous researches are not due to neuroleptic medication. We also propose that this difference in results between the perceptual and the motor tasks may point to a dissociation between corollary discharge for perception and corollary discharge for action.

Habit Learning by Naive Macaques Is Marked by Response Sharpening of Striatal Neurons Representing the Cost and Outcome of Acquired Action Sequences

Over a century of scientific work has focused on defining the factors motivating behavioral learning. Observations in animals and humans trained on a wide range of tasks support reinforcement learning (RL) algorithms as accounting for the learning. Still unknown, however, are the signals that drive learning in naive, untrained subjects. Here, we capitalized on a sequential saccade task in which macaque monkeys acquired repetitive scanning sequences without instruction. We found that spike activity in the caudate nucleus after each trial corresponded to an integrated cost-benefit signal that was highly correlated with the degree of naturalistic untutored learning by the monkeys. Across learning, neurons encoding both cost and outcome gradually acquired increasingly sharp phasic trial-end responses that paralleled the development of the habit-like, repetitive saccade sequences. Our findings demonstrate an integrated cost-benefit signal by which RL and its neural correlates could drive naturalistic behaviors in freely behaving primates.

Contextual factors modulate concurrent planning of sequential saccades.

Natural vision typically involves making multiple eye movements to interpret complex visual scenes. Although previous work has shown that individual saccadic end points are modulated by cognitive context, whether and how contextual factors quantitatively influence the planning of sequential saccades is still unclear. We compared performance of subjects in a modified double-step task under different task instructions (FOLLOW vs. REDIRECT; Ray, Schall, & Murthy, 2004) as well as task structure (40% and 100% FOLLOW). The results support the idea of restricted concurrent preparation when the second saccade was part of the sequence as per task demands as opposed to being inadvertently made following an error. Also, increasing the probability of double-target trials in the task (100% vs. 40% FOLLOW) tended to enhance concurrent planning even when the serial order of saccades continued to remain important. Taken together, these data reveal how the concurrent planning of sequential saccades can be contextually regulated by means of task instruction and trial statistics.