ABSTRACT: Control of saccadic gain is often viewed as a simple compensatory process in which gain is adjusted over many trials by the postsaccadic retinal error, thereby maintaining saccadic accuracy. Here, we propose that gain might also be changed by a reinforcement process not requiring a visual error. To test this hypothesis, we used experimental paradigms in which retinal error was removed by extinguishing the target at the start of each saccade and either an auditory tone or the vision of the target on the fovea was provided as reinforcement after those saccades that met an amplitude criterion. These reinforcement procedures caused a progressive change in saccade amplitude in nearly all subjects, although the rate of adaptation differed greatly among subjects. When we reversed the contingencies and reinforced those saccades landing closer to the original target location, saccade gain changed back toward normal gain in most subjects. When subjects had saccades adapted first by reinforcement and a week later by conventional intrasaccadic step adaptation, both paradigms yielded similar degrees of gain changes and similar transfer to new amplitudes and to new starting positions of the target step as well as comparable rates of recovery. We interpret these changes in saccadic gain in the absence of postsaccadic retinal error as showing that saccade adaptation is not controlled by a single error signal. More generally, our findings suggest that normal saccade adaptation might involve general learning mechanisms rather than only specialized mechanisms for motor calibration.
Project description:Saccadic adaptation is the motor learning process that keeps saccade amplitudes on target. This process is eye position specific: amplitude adaptation that is induced for a saccade at one particular location in the visual field transfers incompletely to saccades at other locations. In our current study, we investigated wether this eye position signal corresponds to the initial or to the final eye position of the saccade. Each case would have different implications on the mechanisms of adaptation. The initial eye position is not directly available, when the adaptation driving post saccadic error signal is received. On the other hand the final eye position signal is not available, when the motor command for the saccade is calculated. In six human subjects we adapted a saccade of 15 degree amplitude that started at a constant position. We then measured the transfer of adaptation to test saccades of 10 and 20 degree amplitude. In each case we compared test saccades that matched the start position of the adapted saccade to those that matched the target of the adapted saccade. We found significantly more transfer of adaptation to test saccades with the same start position than to test saccades with the same target position. The results indicate that saccadic adaptation is specific to the initial eye position. This is consistent with a previously proposed effect of gain field modulated input from areas like the frontal eye field, the lateral intraparietal area and the superior colliculus into the cerebellar adaptation circuitry.
Project description:Whenever we move our eyes, some visual information obtained before a saccade is combined with the visual information obtained after a saccade. Interestingly, saccades rarely land exactly on the saccade target, which may pose a problem for transsaccadic perception as it could affect the quality of postsaccadic input. Recently, however, we showed that transsaccadic feature integration is actually unaffected by deviations of saccade landing points. Possibly, transsaccadic integration remains unaffected because the presaccadic shift of attention follows the intended saccade target and not the actual saccade landing point during regular saccades. Here, we investigated whether saccade landing point errors can in fact alter transsaccadic perception when the presaccadic shift of attention follows the saccade landing point deviation. Given that saccadic adaptation not only changes the saccade vector, but also the presaccadic shift of attention, we combined a feature report paradigm with saccadic adaptation. Observers reported the color of the saccade target, which occasionally changed slightly during a saccade to the target. This task was performed before and after saccadic adaptation. The results showed that, after adaptation, presaccadic color information became less precise and transsaccadic perception had a stronger reliance on the postsaccadic color estimate. Therefore, although previous studies have shown that transsaccadic perception is generally unaffected by saccade landing point deviations, our results reveal that this cannot be considered a general property of the visual system. When presaccadic shifts of attention follow altered saccade landing points, transsaccadic perception is affected, suggesting that transsaccadic feature perception might be dependent on visual spatial attention.
Project description:Eye movements create an ever-changing image of the world on the retina. In particular, frequent saccades call for a compensatory mechanism to transform the changing visual information into a stable percept. To this end, the brain presumably uses internal copies of motor commands. Electrophysiological recordings of visual neurons in the primate lateral intraparietal cortex, the frontal eye fields, and the superior colliculus suggest that the receptive fields (RFs) of special neurons shift towards their post-saccadic positions before the onset of a saccade. However, the perceptual consequences of these shifts remain controversial. We wanted to test in humans whether a remapping of motion adaptation occurs in visual perception.The motion aftereffect (MAE) occurs after viewing of a moving stimulus as an apparent movement to the opposite direction. We designed a saccade paradigm suitable for revealing pre-saccadic remapping of the MAE. Indeed, a transfer of motion adaptation from pre-saccadic to post-saccadic position could be observed when subjects prepared saccades. In the remapping condition, the strength of the MAE was comparable to the effect measured in a control condition (33±7% vs. 27±4%). Contrary, after a saccade or without saccade planning, the MAE was weak or absent when adaptation and test stimulus were located at different retinal locations, i.e. the effect was clearly retinotopic. Regarding visual cognition, our study reveals for the first time predictive remapping of the MAE but no spatiotopic transfer across saccades. Since the cortical sites involved in motion adaptation in primates are most likely the primary visual cortex and the middle temporal area (MT/V5) corresponding to human MT, our results suggest that pre-saccadic remapping extends to these areas, which have been associated with strict retinotopy and therefore with classical RF organization. The pre-saccadic transfer of visual features demonstrated here may be a crucial determinant for a stable percept despite saccades.
Project description:Humans do not notice small displacements to objects that occur during saccades, termed saccadic suppression of displacement (SSD), and this effect is reduced when a blank is introduced between the pre- and postsaccadic stimulus (Bridgeman, Hendry, & Stark, 1975; Deubel, Schneider, & Bridgeman, 1996). While these effects have been studied extensively in adults, it is unclear how these phenomena are characterized in children. A potentially related mechanism, saccadic suppression of contrast sensitivity-a prerequisite to achieve a stable percept-is stronger for children (Bruno, Brambati, Perani, & Morrone, 2006). However, the evidence for how transsaccadic stimulus displacements may be suppressed or integrated is mixed. While they can integrate basic visual feature information from an early age, they cannot integrate multisensory information (Gori, Viva, Sandini, & Burr, 2008; Nardini, Jones, Bedford, & Braddick, 2008), suggesting a failure in the ability to integrate more complex sensory information. We tested children 7 to 12 years old and adults 19 to 23 years old on their ability to perceive intrasaccadic stimulus displacements, with and without a postsaccadic blank. Results showed that children had stronger SSD than adults and a larger blanking effect. Children also had larger undershoots and more variability in their initial saccade endpoints, indicating greater intrinsic uncertainty, and they were faster in executing corrective saccades to account for these errors. Together, these results suggest that children may have a greater internal expectation or prediction of saccade error than adults; thus, the stronger SSD in children may be due to higher intrinsic uncertainty in target localization or saccade execution.
Project description:Adaptation of saccades can be induced by different error signals, such as retinal position errors, prediction errors, or reinforcement learning. Recently, we showed that a shift in the spatial goal of a perceptual task can induce saccadic adaptation, in the absence of a bottom-up position error. Here, we investigated whether this top-down effect is mediated by the visibility of the task-relevant object, by reinforcement due to the feedback about the perceptual judgment or by a target selection mechanism. Participants were asked to discriminate visual stimuli arranged in a vertical compound. To induce adaptation, the discrimination target was presented at eccentric locations in the compound. In the first experiment, we compared adaptation with an easy and difficult discrimination. In the second experiment, we compared adaptation when feedback about the perceptual task was valid and when feedback was provided but was unrelated to performance. In the third experiment, we compared adaptation with instructions to fixate one of the elements in the compound-target selection-to the perceptual task condition-target selection and discrimination. To control for a bottom-up stimulus effect, we ran a fourth experiment in which the only instruction was to look at the compound. The saccade amplitude data were fitted by a two-state model distinguishing between an immediate and a gradual error correction process. We replicated our finding that a perceptual task can drive adaptation of saccades. Adaptation showed no effect of feedback reliability, nor an effect of the perceptual task beyond target selection. Adaptation was induced by a top-down signal since it was absent when there was no target selection instruction and no perceptual task. The immediate error correction was larger for the difficult than for the easy condition, suggesting that task difficulty affects mainly voluntary saccade targeting. In addition, the repetition of experiments one week later increased the magnitude of the gradual error correction. The results dissociate two distinct components of adaptation: an immediate and a gradual error correction. We conclude that perceptual-task induced adaptation is most likely due to top-down target selection within a larger object.
Project description:The improvement of motor behavior, based on experience, is a form of learning that is critically dependent on the cerebellum. A well studied example of cerebellar motor learning is short-term saccadic adaptation (STSA). In STSA, information on saccadic errors is used to improve future saccades. The information optimizing saccade metrics is conveyed by Purkinje cells simple spikes (PC-SS) because they are the critical input to the premotor circuits for saccades. We recorded PC-SS of monkeys undergoing STSA to reveal the code used for improving behavior. We found that the discharge of individual PC-SS was unable to account for the behavioral changes. The PC-SS population burst (PB), however, exhibited changes that closely paralleled the qualitatively different changes of saccade kinematics associated with gain-increase and gain-decrease STSA, respectively. Gain-increase STSA, characterized by an increase in saccade duration, replicates the relationship between saccade duration and the end of the PB valid for unadapted saccades. In contrast, gain-decrease STSA, which sports normal saccade duration but reduced saccadic velocity, is characterized by a PB that ends well before the adapted saccade. This suggests that the duration of normal as well as gain-increased saccades is determined by appropriately setting the end of PB end. However, the duration of gain-decreased saccades is apparently not modified by the cerebellum because the PB signals ends too early to determine saccade end. In summary, STSA, and most probably cerebellar-dependent learning in general, is based on optimizing the shape of a PC-SS population response.
Project description:For humans, visual tracking of moving stimuli often triggers catch-up saccades during smooth pursuit. The switch between these continuous and discrete eye movements is a trade-off between tolerating sustained position error (PE) when no saccade is triggered or a transient loss of vision during the saccade due to saccadic suppression. de Brouwer et al. (2002b) demonstrated that catch-up saccades were less likely to occur when the target re-crosses the fovea within 40-180 ms. To date, there is no mechanistic explanation for how the trigger decision is made by the brain. Recently, we proposed a stochastic decision model for saccade triggering during visual tracking (Coutinho et al., 2018) that relies on a probabilistic estimate of predicted PE (PEpred). Informed by model predictions, we hypothesized that saccade trigger time length and variability will increase when pre-saccadic predicted errors are small or visual uncertainty is high (e.g., for blurred targets). Data collected from human participants performing a double step-ramp task showed that large pre-saccadic PEpred (>10°) produced short saccade trigger times regardless of the level of uncertainty while saccade trigger times preceded by small PEpred (<10°) significantly increased in length and variability, and more so for blurred targets. Our model also predicted increased signal-dependent noise (SDN) as retinal slip (RS) increases; in our data, this resulted in longer saccade trigger times and more smooth trials without saccades. In summary, our data supports our hypothesized predicted error-based decision process for coordinating saccades during smooth pursuit.
Project description: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.
Project description:Visual perception is introspectively stable and continuous across eye movements. It has been hypothesized that displacements in retinal input caused by eye movements can be dissociated from displacements in the external world using extra-retinal information, such as a corollary discharge from the oculomotor system. The extra-retinal information can inform the visual system about an upcoming eye movement and accompanying displacements in retinal input. The parietal cortex has been hypothesized to be critically involved in integrating retinal and extra-retinal information. Two tasks have been widely used to assess the quality of this integration: double-step saccades and intra-saccadic displacements. Double-step saccades performed by patients with parietal cortex lesions seemed to show hypometric second saccades. However, recently idea has been refuted by demonstrating that patients with very similar lesions were able to perform the double step saccades, albeit taking multiple saccades to reach the saccade target. So, it seems that extra-retinal information is still available for saccade execution after a lesion to the parietal lobe. Here, we investigated whether extra-retinal signals are also available for perceptual judgements in nine patients with strokes affecting the posterior parietal cortex. We assessed perceptual continuity with the intra-saccadic displacement task. We exploited the increased sensitivity when a small temporal blank is introduced after saccade offset (blank effect). The blank effect is thought to reflect the availability of extra-retinal signals for perceptual judgements. Although patients exhibited a relative difference to control subjects, they still demonstrated the blank effect. The data suggest that a lesion to the posterior parietal cortex (PPC) alters the processing of extra-retinal signals but does not abolish their influence altogether.
Project description:Previous studies have shown that face stimuli elicit extremely fast and involuntary saccadic responses toward them, relative to other categories of visual stimuli. In the present study, we further investigated to what extent face stimuli influence the programming and execution of saccades examining their amplitude. We performed two experiments using a saccadic choice task: two images (one with a face, one with a vehicle) were simultaneously displayed in the left and right visual fields of participants who had to initiate a saccade toward the image (Experiment 1) or toward a cross in the image (Experiment 2) containing a target stimulus (a face or a vehicle). Results revealed shorter saccades toward vehicle than face targets, even if participants were explicitly asked to perform their saccades toward a specific location (Experiment 2). Furthermore, error saccades had smaller amplitude than correct saccades. Further analyses showed that error saccades were interrupted in mid-flight to initiate a concurrently-programmed corrective saccade. Overall, these data suggest that the content of visual stimuli can influence the programming of saccade amplitude, and that efficient online correction of saccades can be performed during the saccadic choice task.