Influence of panoramic cues during prolonged roll-tilt adaptation on the percept of vertical.

The percept of vertical, which mainly relies on vestibular and visual cues, is known to be affected after sustained whole-body roll tilt, mostly at roll positions adjacent to the position of adaptation. Here we ask whether the viewing of panoramic visual cues during the adaptation further influences the percept of the visual vertical. Participants were rotated in the frontal plane to a 90° clockwise tilt position, which was maintained for 4-minutes. During this period, the subject was either kept in darkness, or viewed panoramic pictures that were either veridical (aligned with gravity) or oriented along the body longitudinal axis. Errors of the subsequent subjective visual vertical (SVV), measured at various tilt angles, showed that the adaptation effect of panoramic cues is local, i.e. for a narrow range of tilts in the direction of the adaptation angle. This distortion was found irrespective of the orientation of the panoramic cues. We conclude that sustained exposure to panoramic and vestibular cues does not adapt the subsequent percept of vertical to the direction of the panoramic cue. Rather, our results suggest that sustained panoramic cues affect the SVV by an indirect effect on head orientation, with a 90° periodicity, that interacts with a vestibular cue to determine the percept of vertical.

Perception of the dynamic visual vertical during sinusoidal linear motion.

The vestibular system provides information for spatial orientation. However, this information is ambiguous: because the otoliths sense the gravitoinertial force, they cannot distinguish gravitational and inertial components. As a consequence, prolonged linear acceleration of the head can be interpreted as tilt, referred to as the somatogravic effect. Previous modeling work suggests that the brain disambiguates the otolith signal according to the rules of Bayesian inference, combining noisy canal cues with the a priori assumption that prolonged linear accelerations are unlikely. Within this modeling framework the noise of the vestibular signals affects the dynamic characteristics of the tilt percept during linear whole-body motion. To test this prediction, we devised a novel paradigm to psychometrically characterize the dynamic visual vertical-as a proxy for the tilt percept-during passive sinusoidal linear motion along the interaural axis (0.33 Hz motion frequency, 1.75 m/s2 peak acceleration, 80 cm displacement). While subjects (n=10) kept fixation on a central body-fixed light, a line was briefly flashed (5 ms) at different phases of the motion, the orientation of which had to be judged relative to gravity. Consistent with the model's prediction, subjects showed a phase-dependent modulation of the dynamic visual vertical, with a subject-specific phase shift with respect to the imposed acceleration signal. The magnitude of this modulation was smaller than predicted, suggesting a contribution of nonvestibular signals to the dynamic visual vertical. Despite their dampening effect, our findings may point to a link between the noise components in the vestibular system and the characteristics of dynamic visual vertical.NEW & NOTEWORTHY A fundamental question in neuroscience is how the brain processes vestibular signals to infer the orientation of the body and objects in space. We show that, under sinusoidal linear motion, systematic error patterns appear in the disambiguation of linear acceleration and spatial orientation. We discuss the dynamics of these illusory percepts in terms of a dynamic Bayesian model that combines uncertainty in the vestibular signals with priors based on the natural statistics of head motion.

Decisions in motion: vestibular contributions to saccadic target selection.

The natural world continuously presents us with many opportunities for action, and thus a process of target selection must precede action execution. While there has been considerable progress in understanding target selection in stationary environments, little is known about target selection when we are in motion. Here we investigated the effect of self-motion signals on saccadic target selection in a dynamic environment. Human subjects were sinusoidally translated (f = 0.6 Hz, 30-cm peak-to-peak displacement) along an interaural axis with a vestibular sled. During the motion two visual targets were presented asynchronously but equidistantly on either side of fixation. Subjects had to look at one of these targets as quickly as possible. With an adaptive approach, the time delay between these targets was adjusted until the subject selected both targets equally often. We determined this balanced time delay for different phases of the motion in order to distinguish the effects of body acceleration and velocity on saccadic target selection. Results show that acceleration (or position, as these are indistinguishable during sinusoidal motion), but not velocity, affects target selection for saccades. Subjects preferred to look at targets in the direction of the acceleration-the leftward target was preferred when the sled accelerated to the left, and vice versa. Saccadic reaction times mimicked this selection bias by being reliably shorter to targets in the direction of acceleration. Our results provide evidence that saccade target selection mechanisms are modulated by self-motion signals, which could be derived directly from the otolith system.

Generalization and transfer of contextual cues in motor learning.

We continuously adapt our movements in daily life, forming new internal models whenever necessary and updating existing ones. Recent work has suggested that this flexibility is enabled via sensorimotor cues, serving to access the correct internal model whenever necessary and keeping new models apart from previous ones. While research to date has mainly focused on identifying the nature of such cue representations, here we investigated whether and how these cue representations generalize, interfere, and transfer within and across effector systems. Subjects were trained to make two-stage reaching movements: a premovement that served as a cue, followed by a targeted movement that was perturbed by one of two opposite curl force fields. The direction of the premovement was uniquely coupled to the direction of the ensuing force field, enabling simultaneous learning of the two respective internal models. After training, generalization of the two premovement cues' representations was tested at untrained premovement directions, within both the trained and untrained hand. We show that the individual premovement representations generalize in a Gaussian-like pattern around the trained premovement direction. When the force fields are of unequal strengths, the cue-dependent generalization skews toward the strongest field. Furthermore, generalization patterns transfer to the nontrained hand, in an extrinsic reference frame. We conclude that contextual cues do not serve as discrete switches between multiple internal models. Instead, their generalization suggests a weighted contribution of the associated internal models based on the angular separation from the trained cues to the net motor output.

Parallax-sensitive remapping of visual space in occipito-parietal alpha-band activity during whole-body motion.

Despite the constantly changing retinal image due to eye, head, and body movements, we are able to maintain a stable representation of the visual environment. Various studies on retinal image shifts caused by saccades have suggested that occipital and parietal areas correct for these perturbations by a gaze-centered remapping of the neural image. However, such a uniform, rotational, remapping mechanism cannot work during translations when objects shift on the retina in a more complex, depth-dependent fashion due to motion parallax. Here we tested whether the brain's activity patterns show parallax-sensitive remapping of remembered visual space during whole-body motion. Under continuous recording of electroencephalography (EEG), we passively translated human subjects while they had to remember the location of a world-fixed visual target, briefly presented in front of or behind the eyes' fixation point prior to the motion. Using a psychometric approach we assessed the quality of the memory update, which had to be made based on vestibular feedback and other extraretinal motion cues. All subjects showed a variable amount of parallax-sensitive updating errors, i.e., the direction of the errors depended on the depth of the target relative to fixation. The EEG recordings show a neural correlate of this parallax-sensitive remapping in the alpha-band power at occipito-parietal electrodes. At parietal electrodes, the strength of these alpha-band modulations correlated significantly with updating performance. These results suggest that alpha-band oscillatory activity reflects the time-varying updating of gaze-centered spatial information during parallax-sensitive remapping during whole-body motion.

Vestibular benefits to task savings in motor adaptation.

In everyday life, we seamlessly adapt our movements and consolidate them to multiple behavioral contexts. This natural flexibility seems to be contingent on the presence of movement-related sensorimotor cues and cannot be reproduced when static visual or haptic cues are given to signify different behavioral contexts. So far, only sensorimotor cues that dissociate the sensorimotor plans prior to force field exposure have been successful in learning two opposing perturbations. Here we show that vestibular cues, which are only available during the perturbation, improve the formation and recall of multiple control strategies. We exposed subjects to inertial forces by accelerating them laterally on a vestibular platform. The coupling between reaching movement (forward-backward) and acceleration direction (leftward-rightward) switched every 160 trials, resulting in two opposite force environments. When exposed for a second time to the same environment, with the opposite environment in between, subjects showed retention resulting in an ∼3 times faster adaptation rate compared with the first exposure. Our results suggest that vestibular cues provide contextual information throughout the reach, which is used to facilitate independent learning and recall of multiple motor memories. Vestibular cues provide feedback about the underlying cause of reach errors, thereby disambiguating the various task environments and reducing interference of motor memories.

Saccadic updating of object orientation for grasping movements.

Reach and grasp movements are a fundamental part of our daily interactions with the environment. This spatially-guided behavior is often directed to memorized objects because of intervening eye movements that caused them to disappear from sight. How does the brain store and maintain the spatial representations of objects for future reach and grasp movements? We had subjects (n=8) make reach and two-digit grasp movements to memorized objects, briefly presented before an intervening saccade. Grasp errors, characterizing the spatial representation of object orientation, depended on current gaze position, with and without intervening saccade. This suggests that the orientation information of the object is coded and updated relative to gaze during intervening saccades, and that the grasp errors arose after the updating stage, during the later transformations involved in grasping. The pattern of reach errors also revealed a gaze-centered updating of object location, consistent with previous literature on updating of single-point targets. Furthermore, grasp and reach errors correlated strongly, but their relationship had a non-unity slope, which may suggest that the gaze-centered spatial updates were made in separate channels. Finally, the errors of the two digits were strongly correlated, supporting the notion that these were not controlled independently to form the grip in these experimental conditions. Taken together, our results suggest that the visuomotor system dynamically represents the short-term memory of location and orientation information for reach-and-grasp movements.

Fatigue-induced changes of impedance and performance in target tracking.

Kinematic variability is caused, in part, by force fluctuations. It has been shown empirically and numerically that the effects of force fluctuations on kinematics can be suppressed by increasing joint impedance. Given that force variability increases with muscular fatigue, we hypothesized that joint impedance would increase with fatigue to retain a prescribed accuracy level. To test this hypothesis, subjects tracked a target by elbow flexion and extension both with fatigued and unfatigued elbow flexor and extensor muscles. Joint impedance was estimated from controlled perturbations to the elbow. Contrary to the hypothesis, elbow impedance decreased, whereas performance, expressed as the time-on-target, was unaffected by fatigue. Further analysis of the data revealed that subjects changed their control strategy with increasing fatigue. Although their overall kinematic variability increased, task performance was retained by staying closer to the center of the target when fatigued. In conclusion, the present study reveals a limitation of impedance modulation in the control of movement variability.