Gaze control during reaching is flexibly modulated to optimize task outcome.

When reaching for an object with the hand, the gaze is usually directed at the target. In a laboratory setting, fixation is strongly maintained at the reach target until the reaching is completed, a phenomenon known as "gaze anchoring." While conventional accounts of such tight eye-hand coordination have often emphasized the internal synergetic linkage between both motor systems, more recent optimal control theories regard motor coordination as the adaptive solution to task requirements. We here investigated to what degree gaze control during reaching is modulated by task demands. We adopted a gaze-anchoring paradigm in which participants had to reach for a target location. During the reach, they additionally had to make a saccadic eye movement to a salient visual cue presented at locations other than the target. We manipulated the task demands by independently changing reward contingencies for saccade reaction time (RT) and reaching accuracy. On average, both saccade RTs and reach error varied systematically with reward condition, with reach accuracy improving when the saccade was delayed. The distribution of the saccade RTs showed two types of eye movements: fast saccades with short RTs, and voluntary saccade with longer RTs. Increased reward for high reach accuracy reduced the probability of fast saccades but left their latency unchanged. The results suggest that gaze anchoring acts through a suppression of fast saccades, a mechanism that can be adaptively adjusted to the current task demands.NEW & NOTEWORTHY During visually guided reaching, our eyes usually fixate the target and saccades elsewhere are delayed ("gaze anchoring"). We here show that the degree of gaze anchoring is flexibly modulated by the reward contingencies of saccade latency and reach accuracy. Reach error became larger when saccades occurred earlier. These results suggest that early saccades are costly for reaching and the brain modulates inhibitory online coordination from the hand to the eye system depending on task requirements.

Online gain update for manual following response accompanied by gaze shift during arm reaching.

To capture objects by hand, online motor corrections are required to compensate for self-body movements. Recent studies have shown that background visual motion, usually caused by body movement, plays a significant role in such online corrections. Visual motion applied during a reaching movement induces a rapid and automatic manual following response (MFR) in the direction of the visual motion. Importantly, the MFR amplitude is modulated by the gaze direction relative to the reach target location (i.e., foveal or peripheral reaching). That is, the brain specifies the adequate visuomotor gain for an online controller based on gaze-reach coordination. However, the time or state point at which the brain specifies this visuomotor gain remains unclear. More specifically, does the gain change occur even during the execution of reaching? In the present study, we measured MFR amplitudes during a task in which the participant performed a saccadic eye movement that altered the gaze-reach coordination during reaching. The results indicate that the MFR amplitude immediately after the saccade termination changed according to the new gaze-reach coordination, suggesting a flexible online updating of the MFR gain during reaching. An additional experiment showed that this gain updating mostly started before the saccade terminated. Therefore, the MFR gain updating process would be triggered by an ocular command related to saccade planning or execution based on forthcoming changes in the gaze-reach coordination. Our findings suggest that the brain flexibly updates the visuomotor gain for an online controller even during reaching movements based on continuous monitoring of the gaze-reach coordination.

The hand sees visual periphery better than the eye: motor-dependent visual motion analyses.

Information pertaining to visual motion is used in the brain not only for conscious perception but also for various kinds of motor controls. In contrast to the increasing amount of evidence supporting the dissociation of visual processing for action versus perception, it is less clear whether the analysis of visual input is shared for characterizing various motor outputs, which require different kinds of interactions with environments. Here we show that, in human visuomotor control, motion analysis for quick hand control is distinct from that for quick eye control in terms of spatiotemporal analysis and spatial integration. The amplitudes of implicit and quick hand and eye responses induced by visual motion stimuli differently varied with stimulus size and pattern smoothness (e.g., spatial frequency). Surprisingly, the hand response did not decrease even when the visual motion with a coarse pattern was mostly occluded over the visual center, whereas the eye response markedly decreased. Since these contrasts cannot be ascribed to any difference in motor dynamics, they clearly indicate different spatial integration of visual motion for the individual motor systems. Going against the overly unified hierarchical view of visual analysis, our data suggest that visual motion analyses are separately tailored from early levels to individual motor modalities. Namely, the hand and eyes see the external world differently.

Body and visual instabilities functionally modulate implicit reaching corrections.

Hierarchical brain-information-processing schemes have frequently assumed that the flexible but slow voluntary action modulates a direct sensorimotor process that can quickly generate a reaction in dynamical interaction. Here we show that the quick visuomotor process for manual movement is modulated by postural and visual instability contexts that are related but remote and prior states to manual movements. A preceding unstable postural context significantly enhanced the reflexive manual response induced by a large-field visual motion during hand reaching while the response was evidently weakened by imposing a preceding random-visual-motion context. These modulations are successfully explained by the Bayesian optimal formulation in which the manual response elicited by visual motion is ascribed to the compensatory response to the estimated self-motion affected by the preceding contextual situations. Our findings suggest an implicit and functional mechanism that links the variability and uncertainty of remote states to the quick sensorimotor transformation.

Gaze-specific motor memories for hand-reaching.

Numerous studies have proposed that our adaptive motor behaviors depend on learning a map between sensory information and limb movement,1-3 called an "internal model." From this perspective, how the brain represents internal models is a critical issue in motor learning, especially regarding their association with spatial frames processed in motor planning.4,5 Extensive experimental evidence suggests that during planning stages for visually guided hand reaching, the brain transforms visual target representations in gaze-centered coordinates to motor commands in limb coordinates, via hand-target vectors in workspace coordinates.6-9 While numerous studies have intensively investigated whether the learning for reaching occurs in workspace or limb coordinates,10-20 the association of the learning with gaze coordinates still remains untested.21 Given the critical role of gaze-related spatial coding in reaching planning,22-26 the potential role of gaze states for learning is worth examining. Here, we show that motor memories for reaching are separately learned according to target location in gaze coordinates. Specifically, two opposing visuomotor rotations, which normally interfere with each other, can be simultaneously learned when each is associated with reaching to a foveal target and peripheral one. We also show that this gaze-dependent learning occurs in force-field adaptation. Furthermore, generalization of gaze-coupled reach adaptation is limited across central, right, and left visual fields. These results suggest that gaze states are available in the formation and recall of multiple internal models for reaching. Our findings provide novel evidence that a gaze-dependent spatial representation can provide a spatial coordinate framework for context-dependent motor learning.

Spatial coincidence of intentional actions modulates an implicit visuomotor control.

We investigated a visuomotor mechanism contributing to reach correction: the manual following response (MFR), which is a quick response to background visual motion that frequently occurs as a reafference when the body moves. Although several visual specificities of the MFR have been elucidated, the functional and computational mechanisms of its motor coordination remain unclear mainly because it involves complex relationships among gaze, reaching target, and visual stimuli. To directly explore how these factors interact in the MFR, we assessed the impact of spatial coincidences among gaze, arm reaching, and visual motion on the MFR. When gaze location was displaced from the reaching target with an identical visual motion kept on the retina, the amplitude of the MFR significantly decreased as displacement increased. A factorial manipulation of gaze, reaching-target, and visual motion locations showed that the response decrease is due to the spatial separation between gaze and reaching target but is not due to the spatial separation between visual motion and reaching target. Additionally, elimination of visual motion around the fovea attenuated the MFR. The effects of these spatial coincidences on the MFR are completely different from their effects on the perceptual mislocalization of targets caused by visual motion. Furthermore, we found clear differences between the modulation sensitivities of the MFR and the ocular following response to spatial mismatch between gaze and reaching locations. These results suggest that the MFR modulation observed in our experiment is not due to changes in visual interaction between target and visual motion or to modulation of motion sensitivity in early visual processing. Instead the motor command of the MFR appears to be modulated by the spatial relationship between gaze and reaching.

Distinct temporal developments of visual motion and position representations for multi-stream visuomotor coordination.

A fundamental but controversial question in information coding of moving visual target is which of 'motion' or 'position' signal is employed in the brain for producing quick motor reactions. Prevailing theory assumed that visually guided reaching is driven always via target position representation influenced by various motion signals (e.g., target texture and surroundings). To rigorously examine this theory, we manipulated the nature of the influence of internal texture motion on the position representation of the target in reaching correction tasks. By focusing on the difference in illusory position shift of targets with the soft- and hard-edges, we succeeded in extracting the temporal development of an indirect effect only ascribed to changes in position representation. Our data revealed that the onset of indirect effect is significantly slower than the adjustment onset itself. This evidence indicates multi-stream processing in visuomotor control: fast and direct contribution of visual motion for quick action initiation, and relatively slow contribution of position representation updated by relevant motion signals for continuous action regulation. The distinctive visuomotor mechanism would be crucial in successfully interacting with time-varying environments in the real world.

The faster you decide, the more accurate localization is possible: Position representation of "curveball illusion" in perception and eye movements.

When the inside texture of a moving object moves, the perceived motion of the object is often distorted toward the direction of the texture's motion (motion-induced position shift), and such perceptual distortion accumulates while the object is watched, causing what is known as the curveball illusion. In a recent study, however, the accumulation of the position error was not observed in saccadic eye movements. Here, we examined whether the position of the illusory object is represented independently in the perceptual and saccadic systems. In the experiments, the stimulus of the curveball illusion was adopted to examine the temporal change in the position representation for saccadic eye movements and for perception by varying the elapsed time from the input of visual information to saccade onset and perceptual judgment, respectively. The results showed that the temporal accumulation of the motion-induced position shift is observed not only in perception but also in saccadic eye movements. In the saccade tasks, the landing positions of saccades gradually shifted to the illusory perceived position as the elapsed time from the target offset to the saccade "go" signal increased. Furthermore, in the perception task, shortening the time between the target offset and the perceptual judgment reduced the size of the illusion effect. Therefore, these results argue against the idea of dissociation between saccadic and perceptual localization of a moving object suggested in the previous study, in which saccades were measured in a rushed way while perceptual responses were measured without time constraint. Instead, the similar temporal trends of these effects imply a common or similar target representation for perception and eye movements which dynamically changes over the course of evidence accumulation.

Disentangling the visual, motor and representational effects of vestibular input.

The body midline provides a basic reference for egocentric representation of external space. Clinical observations have suggested that vestibular information underpins egocentric representations. Here we aimed to clarify whether and how vestibular inputs contribute to egocentric representation in healthy volunteers. In a psychophysical task, participants were asked to judge whether visual stimuli were located to the left or to the right of their body midline. Artificial vestibular stimulation was applied to stimulate the vestibular organs. We found that artificial stimulation of the vestibular system biased body midline perception. Importantly, no effect was found on motor effector selection. We also ruled out additional explanations based on allocentric visual representations and on potential indirect effects caused by vestibular-driven movements of the eyes, head and body. Taken together our data suggest that vestibular information contributes to computation of egocentric representations by affecting the internal representation of the body midline.

Spatiotemporal tuning of rapid interactions between visual-motion analysis and reaching movement.

In addition to the goal-directed preplanned control, which strongly governs reaching movements, another type of control mechanism is suggested by recent findings that arm movements are rapidly entrained by surrounding visual motion. It remains, however, controversial whether this rapid manual response is generated in a goal-oriented manner similarly to preplanned control or is reflexively and directly induced by visual motion. To investigate the sensorimotor process underlying rapid manual responses induced by large-field visual motion, we examined the effects of contrast and spatiotemporal frequency of the visual-motion stimulus. The manual response amplitude increased steeply with image contrast up to 10% and leveled off thereafter. Regardless of the spatial frequency, the response amplitude increased almost proportionally to the logarithm of stimulus speed until the temporal frequency reached 15-20 Hz and then fell off. The maximum response was obtained at the lowest spatial frequency we examined (0.05 cycles/degrees). These stimulus specificities are surprisingly similar to those of the reflexive ocular-following response induced by visual motion, although there is no direct motor entrainment from the ocular to manual responses. In addition, the spatiotemporal tuning is clearly different from that of perceptual effects caused by visual motion. These comparisons suggest that the rapid manual response is generated by a reflexive sensorimotor mechanism. This mechanism shares a distinctive visual-motion processing stage with the reflexive control for other motor systems yet is distinct from visual-motion perception.

Eye-hand coordination in on-line visuomotor adjustments.

When we perform a visually guided reaching action, the brain coordinates our hand and eye movements. Eye-hand coordination has been examined widely, but it remains unclear whether the hand and eye motor systems are coordinated during on-line visuomotor adjustments induced by a target jump during a reaching movement. As such quick motor responses are required when we interact with dynamic environments, eye and hand movements could be coordinated even during on-line motor control. Here, we examine the relationship between online hand adjustment and saccadic eye movement. In contrast to the well-known temporal order of eye and hand initiations where the hand follows the eyes, we found that on-line hand adjustment was initiated before the saccade onset. Despite this order reversal, a correlation between hand and saccade latencies was observed, suggesting that the hand motor system is not independent of eye control even when the hand response was induced before the saccade. Moreover, the latency of the hand adjustment with saccadic eye movement was significantly shorter than that with eye fixation. This hand latency modulation cannot be ascribed to any changes of visual or oculomotor reafferent information as the saccade was not yet initiated when the hand adjustment started. Taken together, the hand motor system would receive preparation signals rather than reafference signals of saccadic eye movements to provide quick manual adjustments of the goal-directed eye-hand movements.