Saccadic Adaptation Research Articles

Competition of salience and informational value in saccadic adaptation

Competition of salience and informational value in saccadic adaptation

Saccadic adaptation driven by attentional selection in visual working memory

Saccadic adaptation driven by attentional selection in visual working memory

Saccade adaptation alters smooth pursuit velocity of small, but not large objects

Saccade adaptation alters smooth pursuit velocity of small, but not large objects

Glissades Are Altered by Lesions to the Oculomotor Vermis but Not by Saccadic Adaptation.

Saccadic eye movements enable fast and precise scanning of the visual field, which is partially controlled by the posterior cerebellar vermis. Textbook saccades have a straight trajectory and a unimodal velocity profile, and hence have well-defined epochs of start and end. However, in practice only a fraction of saccades matches this description. One way in which a saccade can deviate from its trajectory is the presence of an overshoot or undershoot at the end of a saccadic eye movement just before fixation. This additional movement, known as a glissade, is regarded as a motor command error and was characterized decades ago but was almost never studied. Using rhesus macaques, we investigated the properties of glissades and changes to glissade kinematics following cerebellar lesions. Additionally, in monkeys with an intact cerebellum, we investigated whether the glissade amplitude can be modulated using multiple adaptation paradigms. Our results show that saccade kinematics are altered by the presence of a glissade, and that glissades do not appear to have any adaptive function as they do not bring the eye closer to the target. Quantification of these results establishes a detailed description of glissades. Further, we show that lesions to the posterior cerebellum have a deleterious effect on both saccade and glissade properties, which recovers over time. Finally, the saccadic adaptation experiments reveal that glissades cannot be modulated by this training paradigm. Together our work offers a functional study of glissades and provides new insight into the cerebellar involvement in this type of motor error.

A generative learning model for saccade adaptation.

Plasticity in the oculomotor system ensures that saccadic eye movements reliably meet their visual goals—to bring regions of interest into foveal, high-acuity vision. Here, we present a comprehensive description of sensorimotor learning in saccades. We induced continuous adaptation of saccade amplitudes using a double-step paradigm, in which participants saccade to a peripheral target stimulus, which then undergoes a surreptitious, intra-saccadic shift (ISS) as the eyes are in flight. In our experiments, the ISS followed a systematic variation, increasing or decreasing from one saccade to the next as a sinusoidal function of the trial number. Over a large range of frequencies, we confirm that adaptation gain shows (1) a periodic response, reflecting the frequency of the ISS with a delay of a number of trials, and (2) a simultaneous drift towards lower saccade gains. We then show that state-space-based linear time-invariant systems (LTIS) represent suitable generative models for this evolution of saccade gain over time. This state-equation algorithm computes the prediction of an internal (or hidden state-) variable by learning from recent feedback errors, and it can be compared to experimentally observed adaptation gain. The algorithm also includes a forgetting rate that quantifies per-trial leaks in the adaptation gain, as well as a systematic, non-error-based bias. Finally, we study how the parameters of the generative models depend on features of the ISS. Driven by a sinusoidal disturbance, the state-equation admits an exact analytical solution that expresses the parameters of the phenomenological description as functions of those of the generative model. Together with statistical model selection criteria, we use these correspondences to characterize and refine the structure of compatible state-equation models. We discuss the relation of these findings to established results and suggest that they may guide further design of experimental research across domains of sensorimotor adaptation.

A differential role for the posterior cerebellum in the adaptive control of convergence eye movements

IntroductionThe vergence oculomotor system possesses two robust adaptive mechanisms; a fast “dynamic” and a slow “tonic” system that are both vital for single, clear and comfortable binocular vision. The neural substrates underlying these vergence adaptive mechanisms in humans is unclear. MethodsWe investigated the role of the posterior cerebellum in convergence adaptation using inhibitory continuous theta-burst repetitive transcranial magnetic stimulation (cTBS) within a double-blind, sham controlled design while eye movements were recorded at 250hz via infrared oculography. ResultsIn a preliminary experiment we validated our stimulation protocols by reproducing results from previous work on saccadic adaptation during the classic double-step adaptive shortening paradigm. Following this, across a series of three separate experiments we observed a clear dissociation in the effect of cTBS on convergence adaptation. Dynamic adaptation was substantially reduced while tonic adaptation was unaffected. Baseline dynamic fusional vergence response were also unaffected by stimulation. ConclusionsThese results indicate a differential role for the posterior cerebellum in the adaptive control of convergence eye movements and provide initial evidence that repetitive transcranial magnetic stimulation is a viable tool to investigate the neurophysiology of vergence control. The results are discussed in the context of the current models of implicit motor adaptation of vergence and their application to clinical populations and technology design in virtual and augmented head mounted display architectures. Significance statementThe cerebellum plays a critical role in the adaptive control of motor systems. Vergence eye movements shift our gaze in depth allowing us to see in 3D and exhibit two distinct adaptive mechanisms that are engaged under a range of conditions including reading, wearing head-mounted displays and using a new spectacle prescription. It is unclear what role the cerebellum plays in these adaptive mechanisms. To answer this, we temporarily disrupted the function of the posterior cerebellum using non-invasive brain stimulation and report impairment of only one adaptive mechanism, providing evidence for neural compartmentalization. The results have implications for vergence control models and applications to comfort and experience studies in head-mounted displays and the rehabilitation of clinical populations exhibiting vergence dysfunctions.

Inter-individual variability and consistency of saccade adaptation in oblique saccades: Amplitude increase and decrease in the horizontal or vertical saccade component

Despite changes in the physical structures controlling the eyes, saccades, the rapid eye movements used to explore the visual environment, remain accurate throughout the lifetime. The process underlying this sensorimotor adaptation is studied using a double step paradigm: an intra-saccadic target displacement introduces a systematic position error which triggers changes in saccadic amplitude or direction across trials. Numerous researches on this saccade adaptation have been conducted, but the level of inter-individual variability and consistency in saccade gain change and how it relates to increase- or decrease-amplitude paradigms is not fully described. We conducted experiments in four groups of 25 participants with 800 trials per participant, including 200 baseline trials and 200 recovery trials. We used four distinct double-step paradigms that differed by the intra-saccadic target-step leading to either a horizontal (Backward or Forward) or vertical (Upward or Downward) gain modulation. Across experiments 95% of the participants exhibited adaptation, revealing the consistency of this phenomenon. We observed strong inter-individual differences, both in the extent and rate of adaptation, which were not correlated with the individual baseline saccades characteristics. As previously reported, the rates of adaptation were higher for gain decrease than for gain increase experiments but the final extent of adaptation were similar. Our results also support the view that adaptation of oblique saccades occurs where the saccade command is represented as a vector. Finally, at the individual level, we did not observe systematic changes in the saccade metrics in relation to adaptation.

Volitional control of saccadic adaptation.

Saccadic adaptation is assumed to be driven by an unconscious and automatic mechanism. We wondered if the adaptation process is accessible to volitional control, specifically whether any change in saccade gain can be inhibited. Participants were exposed to post-saccadic error by using the double-step paradigm in which a target is presented in a peripheral location and then stepped during the saccade to another location. In one condition, participants were instructed to follow the target step and look at the final target location. In the other condition they were instructed to inhibit the adjustment of saccade amplitude and look at the initial target location. We conducted two experiments, which differed in the size of the intra-saccadic target step. We found that when told to inhibit amplitude adjustment, gain change was close to zero for outward steps, but some adaptation remained for inward steps. Saccadic latency was not affected by the instruction type for inward steps, but when the target was stepped outward, latencies were longer in the inhibition than in the adaptation condition. The results show that volitional control can be exerted on saccadic adaptation. We suggest that volitional control affects the remapping of the target, thus having a larger impact on outward adaptation.

Unconscious Semantic Priming Influences Performance of Visuomotor Tasks Differently but the Effects are Similar in Young and Older Adults

We examined the effects of semantic priming of attention on two sequentially presented visuomotor tasks, traffic judgments and saccadic adaptation. Priming was accomplished with the scrambled sentence task: participants formed meaningful sentences from a list of words where a word denoting wide attention focus was involved. The results showed that semantic priming influenced positively saccade adaptation (its’ benefit increased) while it attenuated visuomotor performance in the traffic task (RT of hand movements increased). We found the effects of priming on both tasks’ performance to be comparable in young and older participants. It was suggested that semantic priming effect on visuomotor tasks depended on the cognitive resources which were needful as for the priming as for the primed task.

A neuronal process for adaptive control of primate saccadic system.

In 1980, Dr. Optican established the existence of an adaptive plasticity of saccades and its dependence on the cerebellum with Dr. Robinson. The advantage of saccades is that the neuronal mechanisms underlying their generation have been well established. This knowledge allows us to identify the neuronal elements that participate in saccade adaptation. Briefly, the superior colliculus (SC) produces a saccade command signal, which reaches motoneurons in the abducens nucleus via the brainstem burst generator. The SC saccade command also is sent to the oculomotor vermis (OMV), a saccade-related area of the cerebellar cortex, and finally converges on the same motoneurons via the caudal fastigial nucleus (cFN) and inhibitory burst neurons (IBN). During adaptation, the saccade-related burst of SC neurons does not change; however, the activity of the cerebellum and its downstream targets do. We demonstrate that the SC is the source of the error signal to the OMV, and the error signal increases the probability of complex spike occurrence and decreases simple spike activity in the OMV. This decrease, in turn, is delivered through the cFN and IBN neurons to decrease motoneuron activity and hence saccade amplitude.

Delineating cerebellar mechanisms in DYT11 myoclonus-dystonia.

Recent research has highlighted the role of the cerebellum in the pathophysiology of myoclonus-dystonia syndrome as a result of mutations in the ɛ-sarcoglycan gene (DYT11). Specifically, a cerebellar-dependent saccadic adaptation task is dramatically impaired in this patient group. The objective of this study was to investigate whether saccadic deficits coexist with impairments of limb adaptation to provide a potential mechanism linking cerebellar dysfunction to the movement disorder within symptomatic body regions. Limb adaptation to visuomotor (visual feedback rotated by 30°) and forcefield (force applied by robot to deviate arm) perturbations were examined in 5 patients with DYT11 and 10 aged-matched controls. Patients with DYT11 successfully adapted to both types of perturbation. Modelled and averaged summary metrics that captured adaptation behaviors were equivalent to the control group across conditions. DYT11 is not characterized by a uniform deficit in adaptation. The previously observed large deficit in saccadic adaption is not reflected in an equivalent deficit in limb adaptation in symptomatic body regions. We suggest potential mechanisms at the root of this discordance and identify key research questions that need future study. © 2018 International Parkinson and Movement Disorder Society.

Timing of concurrent visual stimuli determines modulation of saccadic amplitude

The temporal relation of competing visual stimuli may determine the corresponding oculomotor response. In this study we systematically varied the temporal coincidence of two conflicting stimuli and investigated saccades that were elicited from such stimuli. We varied the time of presentation of two identical spatially separated stimuli between 0 and +165 ms and measured the amplitude of the saccade elicited by these stimuli using infrared eye tracking. In the first experiment, all stimuli were shown for 36 ms only. In the second experiment, stimuli remained on the screen until the subsequent stimulus appeared, whereas in the third experiment all stimuli were removed after saccade onset. Up to an interstimulus interval of 82 ms, we found a significant shift of the saccadic endpoint toward the location of the second stimulus as compared to saccades toward the first stimulus alone. The strongest saccadic bias was observed if a stimulus was shown 36 ms after or before another stimulus. In contrast, time intervals longer than 82 ms elicited saccade adaptation-that is, the saccadic landing point gradually moved toward the second location over time. In more than 99% of trials, the second stimulus appeared before the saccade reached its endpoint. The timing of a conflicting stimulus determines the associated saccadic response: Simultaneous presentation of two stimuli results in a saccadic endpoint at an averaged intermediate position, short interstimulus intervals result in a strong shift of the saccadic endpoint toward the location of the second of two consecutive stimuli, and longer interstimulus intervals elicit saccade adaptation. The timing of two stimuli thus is associated with distinct processes, which complement each other in order to provide an optimal oculomotor response.

Saccadic Adaptation Boosts Ongoing Gamma Activity in a Subsequent Visuoattentional Task.

Attention and saccadic adaptation (SA) are critical components of visual perception, the former enhancing sensory processing of selected objects, the latter maintaining the eye movements accuracy toward them. Recent studies propelled the hypothesis of a tight functional coupling between these mechanisms, possibly due to shared neural substrates. Here, we used magnetoencephalography to investigate for the first time the neurophysiological bases of this coupling and of SA per se. We compared visual discrimination performance of 12 healthy subjects before and after SA. Eye movements and magnetic signals were recorded continuously. Analyses focused on gamma band activity (GBA) during the pretarget period of the discrimination and the saccadic tasks. We found that GBA increases after SA. This increase was found in the right hemisphere for both postadaptation saccadic and discrimination tasks. For the latter, GBA also increased in the left hemisphere. We conclude that oculomotor plasticity involves GBA modulation within an extended neural network which persists after SA, suggesting a possible role of gamma oscillations in the coupling between SA and attention.

Cortico-cerebellar network involved in saccade adaptation.

Saccade adaptation is the learning process that ensures that vision and saccades remain calibrated. The central nervous system network involved in these adaptive processes remains unclear because of difficulties in isolating the learning process from the correlated visual and motor processes. Here we imaged the human brain during a novel saccade adaptation paradigm that allowed us to isolate neural signals involved in learning independent of the changes in the amplitude of corrective saccades usually correlated with adaptation. We show that the changes in activation in the ipsiversive cerebellar vermis that track adaptation are not driven by the changes in corrective saccades and thus provide critical supporting evidence for previous findings. Similarly, we find that activation in the dorsomedial wall of the contraversive precuneus mirrors the pattern found in the cerebellum. Finally, we identify dorsolateral and dorsomedial cortical areas in the frontal and parietal lobes that encode the retinal errors following inaccurate saccades used to drive recalibration. Together, these data identify a distributed network of cerebellar and cortical areas and their specific roles in oculomotor learning. NEW & NOTEWORTHY The central nervous system constantly learns from errors and adapts to keep visual targets and saccades in registration. We imaged the human brain while the gain of saccades adapted to a visual target that was displaced while the eye was in motion, inducing retinal error. Activity in the cerebellum and precuneus tracked learning, whereas parts of the dorsolateral and dorsomedial frontal and parietal cortex encoded the retinal error used to drive learning.

Elimination of the error signal in the superior colliculus impairs saccade motor learning

When movements become dysmetric, the resultant motor error induces a plastic change in the cerebellum to correct the movement, i.e., motor adaptation. Current evidence suggests that the error signal to the cerebellum is delivered by complex spikes originating in the inferior olive (IO). To prove a causal link between the IO error signal and motor adaptation, several studies blocked the IO, which, unfortunately, affected not only the adaptation but also the movement itself. We avoided this confound by inactivating the source of an error signal to the IO. Several studies implicate the superior colliculus (SC) as the source of the error signal to the IO for saccade adaptation. When we inactivated the SC, the metrics of the saccade to be adapted were unchanged, but saccade adaptation was impaired. Thus, an intact rostral SC is necessary for saccade adaptation. Our data provide experimental evidence for the cerebellar learning theory that requires an error signal to drive motor adaptation.

The human saccadic adaptation field across time

The human saccadic adaptation field across time

Localization errors following saccadic adaptation to a dichoptic step

Localization errors following saccadic adaptation to a dichoptic step

Signals driving the adaptation of saccades that require spatial updating.

Saccades adapt to persistent natural or artificially imposed dysmetrias. The characteristics and circuitry of saccade adaptation have been revealed using a visually guided task (VGT) where the vectors of the target step and the intended saccade command are the same. However, in real life, another saccade occasionally intervenes before the saccade to the target occurs. This necessitates an updating of the intended saccade to account for the intervening saccadic displacement, which dissociates the visual target signal and the intended saccade command. We determined whether the adaptation process is similar for VGT and updated saccades by studying the transfer of adaptation between them. The ultimate visual target was dissociated from the intended saccade command with double-step saccade tasks (DSTs) in which two targets are flashed sequentially at different locations while the monkey maintains fixation. The resulting saccades toward the first and second targets occur in the dark. The transfer of visually guided saccade adaptation to the second saccades of a DST and vice versa depended on the eccentricity of the second visual target, and not the second saccade command. If a target with the same eccentricity as the adapted target appears briefly during the intersaccadic interval of a DST, more adaptation transfers. Because a brief appearance of the visual target either before the first saccade or during the intersaccadic interval influences how much adaptation transfer the second saccade will express, the processing of adaptation and DST updating may overlap. NEW & NOTEWORTHY Adaptation and the spatial updating of saccades are thought to be independent processes. When we dissociate the visual target and the intended saccade command, the transfer of visually guided saccade adaptation to the saccades of the double-step saccade tasks (DST) and vice versa is driven by a visual not motor error. The visual target has an effect until the second saccade of a DST occurs. Therefore, the processing of adaptation and the spatial updating of saccades may overlap.

Cerebellar transcranial direct current stimulation interacts with BDNF Val66Met in motor learning

BackgroundCerebellar transcranial direct current stimulation has been reported to enhance motor associative learning and motor adaptation, holding promise for clinical application in patients with movement disorders. However, behavioral benefits from cerebellar tDCS have been inconsistent. ObjectiveIdentifying determinants of treatment success is necessary. BDNF Val66Met is a candidate determinant, because the polymorphism is associated with motor skill learning and BDNF is thought to mediate tDCS effects. MethodsWe undertook two cerebellar tDCS studies in subjects genotyped for BDNF Val66Met. Subjects performed an eyeblink conditioning task and received sham, anodal or cathodal tDCS (N = 117, between-subjects design) or a vestibulo-ocular reflex adaptation task and received sham and anodal tDCS (N = 51 subjects, within-subjects design). Performance was quantified as a learning parameter from 0 to 100%. We investigated (1) the distribution of the learning parameter with mixture modeling presented as the mean (M), standard deviation (S) and proportion (P) of the groups, and (2) the role of BDNF Val66Met and cerebellar tDCS using linear regression presented as the regression coefficients (B) and odds ratios (OR) with equally-tailed intervals (ETIs). ResultsFor the eyeblink conditioning task, we found distinct groups of learners (MLearner = 67.2%; SLearner = 14.7%; PLearner = 61.6%) and non-learners (MNon-learner = 14.2%; SNon-learner = 8.0%; PNon-learner = 38.4%). Carriers of the BDNF Val66Met polymorphism were more likely to be learners (OR = 2.7 [1.2 6.2]). Within the group of learners, anodal tDCS supported eyeblink conditioning in BDNF Val66Met non-carriers (B = 11.9% 95%ETI = [0.8 23.0]%), but not in carriers (B = 1.0% 95%ETI = [-10.2 12.1]%). For the vestibulo-ocular reflex adaptation task, we found no effect of BDNF Val66Met (B = −2.0% 95%ETI = [-8.7 4.7]%) or anodal tDCS in either carriers (B = 3.4% 95%ETI = [-3.2 9.5]%) or non-carriers (B = 0.6% 95%ETI = [-3.4 4.8]%). Finally, we performed additional saccade and visuomotor adaptation experiments (N = 72) to investigate the general role of BDNF Val66Met in cerebellum-dependent learning and found no difference between carriers and non-carriers for both saccade (B = 1.0% 95%ETI = [-8.6 10.6]%) and visuomotor adaptation (B = 2.7% 95%ETI = [-2.5 7.9]%). ConclusionsThe specific role for BDNF Val66Met in eyeblink conditioning, but not vestibulo-ocular reflex adaptation, saccade adaptation or visuomotor adaptation could be related to dominance of the role of simple spike suppression of cerebellar Purkinje cells with a high baseline firing frequency in eyeblink conditioning. Susceptibility of non-carriers to anodal tDCS in eyeblink conditioning might be explained by a relatively larger effect of tDCS-induced subthreshold depolarization in this group, which might increase the spontaneous firing frequency up to the level of that of the carriers.

Psychosocial stress affects the acquisition of cerebellar-dependent sensorimotor adaptation

Despite being overlooked in theoretical models of stress-related disorders, differences in cerebellar structure and function are consistently reported in studies of individuals exposed to current and early-life stressors. However, the mediating processes through which stress impacts upon cerebellar function are currently unknown. The aim of the current experiment was to test the effects of experimentally-induced acute stress on cerebellar functioning, using a classic, forward saccadic adaptation paradigm in healthy, young men and women. Stress induction was achieved by employing the Montreal Imaging Stress Task (MIST), a task employing mental arithmetic and negative social feedback to generate significant physiological and endocrine stress responses. Saccadic adaptation was elicited using the double-step target paradigm. In the experiment, 48 participants matched for gender and age were exposed to either a stress (n = 25) or a control (n = 23) condition. Saliva for cortisol analysis was collected before, immediately after, and 10, and 30 min after the MIST. Saccadic adaptation was assessed approximately 10 min after stress induction, when cortisol levels peaked. Participants in the stress group reported significantly more stress symptoms and exhibited greater total cortisol output compared to controls. The stress manipulation was associated with slower learning rates in the stress group, while control participants acquired adaptation faster. Learning rates were negatively associated with cortisol output and mood disturbance. Results suggest that experimentally-induced stress slowed acquisition of cerebellar-dependent saccadic adaptation, related to increases in cortisol output. These ‘proof-of-principle’ data demonstrate that stress modulates cerebellar-related functions.