Saccadic Adaptation Research Articles

Saccades to both vision and touch are modified following adaptation but cross-modal transfers are asymmetrical.

Adaptation of reactive saccades (RS), made toward the sudden appearance of stimuli in our environment, is a plastic mechanism thought to occur at the motor level of saccade generation. As saccadic oculomotor commands integrate multisensory information in the parietal cortex and superior colliculus, adaptation of RS should occur not only toward visual but also tactile targets. In addition, saccadic adaptation in one modality (vision or touch) should transfer cross-modally. To test these predictions, we used the double-step target paradigm to adapt rightward saccades made at two different eccentricities toward the participants' index and middle fingers, identified either visually (experiment 1) or tactually (experiment 2). In each experiment, the rate of adaptation induced for the adapted modality and the rate of adaptation transfer to the nonadapted modality were compared with that measured in a control (no adaptation) session. Results revealed that touch-triggered RS can be adapted as well as visually triggered ones. Moreover, the transfer pattern was asymmetric: visual saccadic adaptation transferred fully to tactile saccades, whereas tactile saccadic adaptation, despite full generalization to nonadapted fingers, transferred only partially to visual saccades. These findings disclose that in the case of tactile saccades, adaptation can be elicited in the absence of postsaccadic visual feedback. In addition, the asymmetric adaptation transfer across sensory modalities suggests that the adaptation locus for tactile saccades may occur in part upstream of the final motor pathway common to all saccades. These findings bring new insights both on the functional loci(us) and on the error signals of RS adaptation. NEW & NOTEWORTHY The present study revealed that, as predicted from a large literature, adaptation of visual reactive saccades transfers to tactile saccades of the same as well as neighboring amplitudes. Furthermore, in a modified double-step target paradigm, tactile saccades exposed to repeated errors adapt with a similar rate and spatial generalization as visual saccades, but this adaptation only slightly transfers to visual saccades. These findings bring new information on saccadic adaptation processes.

Contextual saccadic adaptation : you can see it but you can’t learn from it

Contextual saccadic adaptation : you can see it but you can’t learn from it

Comparison of adaptation characteristics between visually and memory-guided saccades.

Saccade adaptation plays a crucial role in maintaining saccade accuracy. The behavioral characteristics and neural mechanisms of saccade adaptation for an externally cued movement, such as visually guided saccades (VGS), are well studied in nonhuman primates. In contrast, little is known about the saccade adaptation of an internally driven movement, such as memory-guided saccades (MGS), which are guided by visuospatial working memory. As the oculomotor plant changes because of growth, aging, or skeletomuscular problems, both types of saccades need to be adapted. Do both saccade types engage a common adaptation mechanism? In this study, we compared the characteristics of amplitude decrease adaptation in MGS with VGS in nonhuman primates. We found that the adaptation speed was faster for MGS than for VGS. Saccade duration changed during MGS adaptation, whereas saccade peak velocity changed during VGS adaptation. We also compared the adaptation field, that is, the gain change for saccade amplitudes other than the adapted. The gain change for MGS declines on both smaller and larger sides of adapted amplitude, more rapidly for larger than smaller amplitudes, whereas the decline in VGS was reversed. Thus, the differences between VGS and MGS adaptation characteristics support the previously suggested hypothesis that the adaptation mechanisms of VGS and MGS are distinct. Furthermore, the result suggests that the MGS adaptation site is a brain structure that influences saccade duration, whereas the VGS adaptation site influences saccade peak velocity. These results should be beneficial for future neurophysiological experiments.NEW & NOTEWORTHY Plasticity helps to overcome persistent motor errors. Such motor plasticity or adaptation can be investigated with saccades. Thus far our knowledge is primarily about visually guided saccades, an externally cued movement, which we can make only when the object is visible at the time of saccade. However, as the world is complex, we can make saccades even when the object is not visible. Here, we investigate the adaptation of an internally driven movement: the memory-guided saccade.

Impaired saccadic adaptation as a biomarker for disease status in pre- and early symptomatic Huntington's disease

Impaired saccadic adaptation as a biomarker for disease status in pre- and early symptomatic Huntington's disease

No evidence for differential saccadic adaptation in children and adults with an autism spectrum diagnosis.

Altered patterns of eye-movements during scene exploration, and atypical gaze preferences in social settings, have long been noted as features of the Autism phenotype. While these are typically attributed to differences in social engagement and interests (e.g., preferences for inanimate objects over face stimuli), there are also reports of differential saccade measures to non-social stimuli, raising the possibility that fundamental differences in visuo-sensorimotor processing may be at play. Here, we tested the plasticity of the eye-movement system using a classic saccade-adaptation paradigm to assess whether individuals with ASD make typical adjustments to their eye-movements in response to experimentally introduced errors. Saccade adaptation can be measured in infants as young as 10 months, raising the possibility that such measures could be useful as early neuro-markers of ASD risk. Saccade amplitudes were measured while children and adults with ASD (N = 41) and age-matched typically developing (TD) individuals (N = 68) made rapid eye-movements to peripherally presented targets. During adaptation trials, the target was relocated from 20-degrees to 15-degrees from fixation once a saccade to the original target location was initiated, a manipulation that leads to systematic reduction in saccade amplitudes in typical observers. Neither children nor adults with ASD showed any differences relative to TD peers in their abilities to appropriately adapt saccades in the face of persistently introduced errors. Of the three studies to date of saccade adaptation in ASD, none have shown deficits in saccade adaptation that are sufficient to generalize to the whole or a subgroup of the ASD population. Unlike prior studies, we found no evidence for a slower adaptation rate during the early adaptation phase, and no of evidence greater variance of saccade amplitudes in ASD. In post hoc analysis, there was evidence for larger primary saccades to non-adapted targets, a finding requiring replication in future work.

Impairments of saccadic and reaching adaptation in essential tremor are linked to movement execution.

Essential tremor (ET) is a neurological disorder characterized by involuntary oscillations of the limbs. Previous studies have hypothesized that ET is a cerebellar disorder and reported impairments in motor adaptation. However, recent advances have highlighted that motor adaptation involves several components linked to anticipation and control, all dependent on cerebellum. We studied the contribution of both components in adaptation to better understand the adaptation impairments observed in ET from a behavioral perspective. To address this question, we investigated behavioral markers of adaptation in ET patients (n = 20) and age-matched neurologically intact volunteers (n = 20) in saccadic and upper limb adaptation tasks, probing compensation for target jumps and for velocity-dependent force fields, respectively. We found that both groups adapted their movements to the novel contexts; however, ET patients adapted to a lesser extent compared with neurologically intact volunteers. Importantly, components of the movement linked to anticipation were preserved in the ET group, whereas components linked to movement execution appeared responsible for the adaptation deficit in this group. Altogether, our results suggest that execution deficits may be a specific functional consequence of the alteration of neural pathways associated with ET.NEW & NOTEWORTHY We tested essential tremor patients' adaptation abilities in classical tasks including saccadic adaptation to target jumps and reaching adaptation to force field disturbances. Patients' adaptation was present but impaired in both tasks. Interestingly, the deficits were mainly present during movement execution, whereas the anticipatory components of movements were similar to neurologically intact volunteers. These findings reinforce the hypothesis of a cerebellar origin for essential tremor and detail the motor adaptation impairments previously found in this disorder.

Activity of the Substantia Nigra pars Reticulata During Saccade Adaptation.

When movements become inaccurate, the resultant error induces motor adaptation to improve accuracy. This error-based motor learning is regarded as a cerebellar function. However, the influence of the other brain areas on adaptation is poorly understood. During saccade adaptation, a type of error-based motor learning, the superior colliculus (SC) sends a post-saccadic error signal to the cerebellum to drive adaptation. Since the SC is directly inhibited by the substantia nigra pars reticulata (SNr), we hypothesized that the SNr might influence saccade adaptation by affecting the SC error signal. In fact, previous studies indicated that the SNr encodes motivation and motivation influences saccade adaptation. In this study, we first established that the SNr projects to the rostral SC, where small error signals are generated, in non-human primates. Then, we examined SNr activity while the animal underwent adaptation. SNr neurons paused their activity in association with the error. This pause was shallower and delayed compared to those of no-error trial saccades. The pause at the end of the adaptation was shallower and delayed compared to that at the beginning of the adaptation. The change in the inter-trial interval, an indicator of motivation, and adaptation speed had a positive correlation with the changes in the error-related pause. These results suggest that 1: the SNr exhibits a unique activity pattern during the error interval, 2: SNr activity increases during adaptation, consistent with the decrease in SC activity, and 3: motivational decay during the adaptation session might increase SNr activity and influence the adaptation speed.Significance StatementMovements impaired due to stroke, injury, or aging recover gradually. To repair an inaccurate movement, the brain measures the error of the movement and changes the movement to minimize the error. This process is called motor adaptation. Although it has been established that the cerebellum plays an essential role in this adaptation, the influence of the other brain areas on the adaptation process is not well defined. The observation that motivation levels influence adaptation led us to suspect that the basal ganglia may influence adaptation. Here, we reveal the substantia nigra pars reticulata activity changes during saccade adaptation in monkeys and suggest how the basal ganglia influence the error signal.

Altered oculomotor flexibility is linked to high autistic traits

Autism is a multifaced disorder comprising sensory abnormalities and a general inflexibility in the motor domain. The sensorimotor system is continuously challenged to answer whether motion-contingent errors result from own movements or whether they are due to external motion. Disturbances in this decision could lead to the perception of motion when there is none and to an inflexibility with regard to motor learning. Here, we test the hypothesis that altered processing of gaze-contingent sensations are responsible for both the motor inflexibility and the sensory overload in autism. We measured motor flexibility by testing how strong participants adapted in a classical saccade adaptation task. We asked healthy participants, scored for autistic traits, to make saccades to a target that was displaced either in inward or in outward direction during saccade execution. The amount of saccade adaptation, that requires to shift the internal target representation, varied with the autistic symptom severity. The higher participants scored for autistic traits, the less they adapted. In order to test for visual stability, we asked participants to localize the position of the saccade target after they completed their saccade. We found the often-reported saccade-induced mis-localization in low Autistic Quotient (AQ) participants. However, we also found mislocalization in high AQ participants despite the absence of saccade adaptation. Our data suggest that high autistic traits are associated with an oculomotor inflexibility that might produce altered processing of trans-saccadic vision which might increase the perceptual overstimulation that is experienced in autism spectrum disorders (ASD).

Does visual uncertainty influence saccadic adaptation?

Does visual uncertainty influence saccadic adaptation?

P.018 Oculomotor learning as a biomarker in Huntington’s Disease (HD) patients

Background: Huntington’s disease (HD) is an inherited neurodegenerative disorder associated with cognitive, psychiatric, and motor dysfunction. As a potential behavioural biomarker, experimental tasks assessing motor learning may thus provide a reasonable assay of HD onset and progression. The saccadic adaptation paradigm is a non-invasive, accessible method of assessing rapid learning in the oculomotor system. Evidence demonstrates that the thalamus and basal ganglia are important loci for saccadic adaptation, also known to exhibit neurodegenerative pathology before the onset of clinically observable symptoms in HD. Methods: 26 early symptomatic HD patients (Total Functional Capacity Score ≥ 10/13) and sex/age-matched controls were tested on a standard saccadic adaptation task. Eye movements were measured using infrared oculography. Learning dynamics of how quickly the participants adapted their saccade metrics were analysed using state learning models. Results: Initial findings demonstrate that the learning dynamics of HD patients are slower and more variable with respect to saccade amplitude compared to controls. Conclusions: These results demonstrate that motor learning dynamics as captured by a saccadic adaptation task reveal early motor dysfunction in HD, thus providing a discriminating tool to detect early pathological changes in HD patients. Further work is needed regarding applications as a biomarker for disease progression.

Adaptive changes to saccade amplitude and target localization do not require pre-saccadic target visibility

The accuracy of saccadic eye movements is maintained by saccadic adaptation, a learning mechanism that is proposed to rely on visual prediction error, i.e., a mismatch between the pre-saccadically predicted and post-saccadically experienced position of the saccade target. However, recent research indicates that saccadic adaptation might be driven by postdictive motor error, i.e., a retrospective estimation of the pre-saccadic target position based on the post-saccadic image. We investigated whether oculomotor behavior can be adapted based on post-saccadic target information alone. We measured eye movements and localization judgements as participants aimed saccades at an initially invisible target, which was always shown only after the saccade. Each such trial was followed by either a pre- or a post-saccadic localization trial. The target position was fixed for the first 100 trials of the experiment and, during the following 200 trials, successively shifted inward or outward. Saccade amplitude and the pre- and post-saccadic localization judgements adjusted to the changing target position. Our results suggest that post-saccadic information is sufficient to induce error-reducing adaptive changes in saccade amplitude and target localization, possibly reflecting continuous updating of the estimated pre-saccadic target location driven by postdictive motor error.

Vision Beyond Vision: Lessons Learned from Amblyopia

ABSTRACT Amblyopia is characterized by spatiotemporal uncertainty in the visual system. In addition to its effects on vision, amblyopia also exerts a widespread impact on other systems. Many of these changes are observed not only during amblyopic eye viewing but also during fellow eye and binocular viewing. They generally correlate with the severity of visual acuity and stereo acuity loss. The affected systems include: (1) oculomotor control manifested as abnormal fixation, saccades, smooth pursuit, and saccadic adaptation; (2) motor control with altered programming, execution, and temporal dynamics of eye-hand coordination, and decreased ability of the sensorimotor system to adapt to changes in the visual environment; (3) balance control with decreased postural stability; (4) multisensory integration characterized by reduced McGurk effect and altered cross-modal interactions in audiovisual perception; and (5) auditory localization manifested as impaired spatial hearing as a result of abnormal developmental calibration of the auditory map. To detect amblyopia early, a targeted approach is required to identify children from low-income families through in-school visual screening, supplemented by follow-up care and free eyeglasses in high-needs schools.

Motor recalibration of visual and saccadic maps.

How does the brain maintain an accurate visual representation of external space? Movement errors following saccade execution provide sufficient information to recalibrate motor and visual space. Here, we asked whether spatial information for vision and saccades is processed in shared or in separate resources. We used saccade adaptation to modify both, saccade amplitudes and visual mislocalization. After saccade adaptation was induced, we compared participants' saccadic and perceptual localization before and after we inserted 'no error' trials. In these trials, we clamped the post-saccadic error online to the predicted endpoints of saccades. In separate experiments, we either annulled the retinal or the prediction error. We also varied the number of 'no error' trials across conditions. In all conditions, we found that saccade adaptation remained undisturbed by the insertion of 'no error' trials. However, mislocalization decreased as a function of the number of trials in which zero retinal error was displayed. When the prediction error was clamped to zero, no mislocalization was observed at all. The results demonstrate the post-saccadic error is used separately to recalibrate visual and saccadic space.

Interaction of dynamic error signals in saccade adaptation.

Motor adaptation maintains movement accuracy. To evaluate movement accuracy, motor adaptation relies on an error signal, generated by the movement target, while suppressing error signals from irrelevant objects in the vicinity. Previous work used static testing environments, where all information required to evaluate movement accuracy was available simultaneously. Using saccadic eye movements as a model for motor adaptation, we tested how movement accuracy is maintained in dynamic environments, where the availability of conflicting error signals varied over time. Participants made a vertical saccade toward a target (either a small square or a large ring). Upon saccade detection, two candidate stimuli were shown left and right of the target, and participants were instructed to discriminate a feature on one of the candidates. Critically, candidate stimuli were presented sequentially, and saccade adaptation, thus, had to resolve a conflict between a task-relevant and a task-irrelevant error signal that were separated in space and time. We found that the saccade target influenced several aspects of oculomotor learning. In presence of a small target, saccade adaptation evaluated movement accuracy based on the first available error signal after the saccade, irrespective of its task relevance. However, a large target not only allowed for greater flexibility when evaluating movement accuracy, but it also promoted a stronger contribution of strategic behavior when compensating inaccurate saccades. Our results demonstrate how motor adaptation maintains movement accuracy in dynamic environments, and how properties of the visual environment modulate the relative contribution of different learning processes.NEW & NOTEWORTHY Motor adaptation is typically studied in static environments, where all information that is required to evaluate movement accuracy is available simultaneously. Here, using saccadic eye movements as a model, we studied motor adaptation in a dynamic environment, where the availability of conflicting information about movement accuracy varied over time. We demonstrate that properties of the visual environment determine how dynamic movement errors are corrected.

Decoding Trans-Saccadic Prediction Error.

We are constantly sampling our environment by moving our eyes, but our subjective experience of the world is stable and constant. Stimulus displacement during or shortly after a saccade often goes unnoticed, a phenomenon called the saccadic suppression of displacement. Although we fail to notice such displacements, our oculomotor system computes the prediction errors and adequately adjusts the gaze and future saccadic execution, a phenomenon known as saccadic adaptation. In the present study, we aimed to find a brain signature of the trans-saccadic prediction error that informs the motor system but not explicit perception. We asked participants (either sex) to report whether a visual target was displaced during a saccade while recording electroencephalography (EEG). Using multivariate pattern analysis, we were able to differentiate displacements from no displacements, even when participants failed to report the displacement. In other words, we found that trans-saccadic prediction error is represented in the EEG signal 100 ms after the displacement presentation, mainly in occipital and parieto-occipital channels, even in the absence of explicit perception of the displacement.SIGNIFICANCE STATEMENT Stability in vision occurs even while performing saccades. One suggested mechanism for this counterintuitive visual phenomenon is that external displacement is suppressed during the retinal remapping caused by a saccade. Here, we shed light on the mechanisms of trans-saccadic stability by showing that displacement information is not entirely suppressed and specifically present in the early stages of visual processing. Such a signal is relevant and computed for oculomotor adjustment despite being neglected for perception.

Interaction of dynamic error signals in saccade adaptation

Interaction of dynamic error signals in saccade adaptation

Interaction of dynamic error signals in saccade adaptation

Interaction of dynamic error signals in saccade adaptation

Neural substrates of saccadic adaptation: Plastic changes versus error processing and forward versus backward learning

Previous behavioral, clinical, and neuroimaging studies suggest that the neural substrates of adaptation of saccadic eye movements involve, beyond the central role of the cerebellum, several, still incompletely determined, cortical areas. Furthermore, no neuroimaging study has yet tackled the differences between saccade lengthening (“forward adaptation”) and shortening (“backward adaptation”) and neither between their two main components, i.e. error processing and oculomotor changes. The present fMRI study was designed to fill these gaps. Blood-oxygen-level-dependent (BOLD) signal and eye movements of 24 healthy volunteers were acquired while performing reactive saccades under 4 conditions repeated in short blocks of 16 trials: systematic target jump during the saccade and in the saccade direction (forward: FW) or in the opposite direction (backward: BW), randomly directed FW or BW target jump during the saccade (random: RND) and no intra-saccadic target jump (stationary: STA). BOLD signals were analyzed both through general linear model (GLM) approaches applied at the whole-brain level and through sensitive Multi-Variate Pattern Analyses (MVPA) applied to 34 regions of interest (ROIs) identified from independent 'Saccade Localizer’ functional data. Oculomotor data were consistent with successful induction of forward and backward adaptation in FW and BW blocks, respectively. The different analyses of voxel activation patterns (MVPAs) disclosed the involvement of 1) a set of ROIs specifically related to adaptation in the right occipital cortex, right and left MT/MST, right FEF and right pallidum; 2) several ROIs specifically involved in error signal processing in the left occipital cortex, left PEF, left precuneus, Medial Cingulate cortex (MCC), left inferior and right superior cerebellum; 3) ROIs specific to the direction of adaptation in the occipital cortex and MT/MST (left and right hemispheres for FW and BW, respectively) and in the pallidum of the right hemisphere (FW). The involvement of the left PEF and of the (left and right) occipital cortex were further supported and qualified by the whole brain GLM analysis: clusters of increased activity were found in PEF for the RND versus STA contrast (related to error processing) and in the left (right) occipital cortex for the FW (BW) versus STA contrasts [related to the FW (BW) direction of error and/or adaptation]. The present study both adds complementary data to the growing literature supporting a role of the cerebral cortex in saccadic adaptation through feedback and feedforward relationships with the cerebellum and provides the basis for improving conceptual frameworks of oculomotor plasticity and of its link with spatial cognition.

Mislocalization after inhibition of saccadic adaptation.

Saccadic eye movements are often imprecise and result in an error between expected and actual retinal target location after the saccade. Repeated experience of this error produces changes in saccade amplitude to reduce the error and concomitant changes in apparent visual location. We investigated the relationship between these two plastic processes in a series of experiments. Following a recent paradigm of inhibition of saccadic adaptation, in which participants are instructed to look at the initial target position and to continue to look at that position even if the target were to move again, our participants nevertheless perceived a visual probe presented near the saccade target to be shifted in direction of the target error. The location percept of the target gradually shifted and diverged over time from the executed saccade. Our findings indicate that changes in perceived location can be the same even when changes in saccade amplitude differ according to instruction and can develop even when the amplitude of the saccades executed during the adaptation procedure does not change. There are two possible explanations for this divergence between the adaptation states of saccade amplitude and perceived location. Either the intrasaccadic target step might trigger updating of the association between pre- and post-saccadic target positions, causing the localization shift, or the saccade motor command adjusts together with the perceived location at a common adaptation site, downstream from which voluntary control is exerted upon the executed eye movement only.

Contextual saccade adaptation induced by sequential saccades.

Saccade adaptation is the gradual adjustment of saccade end point to maintain spatial accuracy. Contextual adaptation refers to a situation in which the adaptation-related change in saccade end point is contingent on the behavioral context in which the saccade is made. For example, in some situations, the same saccade to the same retinotopic location can be simultaneously adapted in opposite directions depending on the context in which it is made. Saccade adaptation has traditionally been studied in isolated movements, but in everyday life, saccades are often planned and executed in sequences. The oculomotor system may therefore have adaptive mechanisms specific to sequential saccades. Here, in five experiments, we investigated contextual saccade adaptation in sequences of saccades. In the first experiment, we demonstrate that saccades to a given retinotopic location can be simultaneously adapted in opposite directions depending on whether they occur in isolation or in a sequence. In the other experiments, we measured the extent to which properties of the previous and following saccades in a sequence can induce contextual saccade adaptation. Overall, we find that the existence, direction, and amplitude of previous and subsequent saccades, as well as the order of the current saccade within a movement sequence, can all induce contextual adaptation. These novel findings demonstrate the surprising flexibility of the system in maintaining end point accuracy, and support the idea that saccades made in a movement sequence are planned concurrently rather than independently.NEW & NOTEWORTHY This study reveals a new type of contextual saccade adaptation: sequential saccades are able to induce contextual saccade adaptation when direction, amplitude, or the existence of preceding and following saccades are used as contexts. These novel findings are also consistent with the idea that saccades made in a sequence are planned concurrently rather than independently.