Online corrective responses following target jump in altered gravitoinertial force field point to nested feedforward and feedback control

Studies on goal-directed arm movements have shown a close link between feedforward and feedback control in protocols where both planning and online control processes faced a similar type of perturbation, either mechanical or visual. This particular context might have facilitated the use of an adapted internal model by feedforward and feedback control. Here we considered this link in a context where after feedforward control was adapted through proprioception-based processes, feedback control was tested under visual perturbation. We analyzed the response of the reaching hand to target displacements following adaptation to an altered force field induced by rotating participants at constant velocity. Reaching corrections were assessed through variables related to the accuracy (lateral and longitudinal endpoint errors) and kinematics (movement time, peak velocity) of the corrective movements. The electromyographic activity of different arm muscles (pectoralis, deltoid, biceps and triceps brachii) was analyzed. Statistical analyses revealed that accuracy and kinematics of corrective movements were strikingly alike between normal and altered gravitoinertial force fields. However, pectoralis and biceps muscle activities recorded during corrective movements were significantly modified to counteract the effect of rotation-induced Coriolis and centrifugal forces on the arm. Remarkably, feedback control was functional from the very first time participants encountered a target jump in the altered force field. Overall, the present results demonstrate that feedforward control enables immediate functional feedback control even when applied to distinct sensorimotor processes.

Motion Perception During Variable-Radius Swing Motion in Darkness

Using a variable-radius roll swing motion paradigm, we examined the influence of interaural ( y-axis) and dorsoventral ( z-axis) force modulation on perceived tilt and translation by measuring perception of horizontal translation, roll tilt, and distance from center of rotation (radius) at 0.45 and 0.8 Hz using standard magnitude estimation techniques (primarily verbal reports) in darkness. Results show that motion perception was significantly influenced by both y- and z-axis forces. During constant radius trials, subjects' perceptions of tilt and translation were generally almost veridical. By selectively pairing radius (1.22 and 0.38 m) and frequency (0.45 and 0.8 Hz, respectively), the y-axis acceleration could be tailored in opposition to gravity so that the combined y-axis gravitoinertial force (GIF) variation at the subject's ears was reduced to ∼0.035 m/s2 – in effect, the y-axis GIF was “nulled” below putative perceptual threshold levels. With y-axis force nulling, subjects overestimated their tilt angle and underestimated their horizontal translation and radius. For some y-axis nulling trials, a radial linear acceleration at twice the tilt frequency (0.25 m/s2 at 0.9 Hz, 0.13 m/s2 at 1.6 Hz) was simultaneously applied to reduce the z-axis force variations caused by centripetal acceleration and by changes in the z-axis component of gravity during tilt. For other trials, the phase of this radial linear acceleration was altered to double the magnitude of the z-axis force variations. z-axis force nulling further increased the perceived tilt angle and further decreased perceived horizontal translation and radius relative to the y-axis nulling trials, while z-axis force doubling had the opposite effect. Subject reports were remarkably geometrically consistent; an observer model-based analysis suggests that perception was influenced by knowledge of swing geometry.

Vertical skew due to changes in gravitoinertial force: A possible consequence of otolith asymmetry

During the alternating enhanced and reduced "gravity" levels of parabolic flight, subjects noted that a horizontally eccentric point target viewed binocularly in darkness seemed to split into two targets with vertical divergence. The amount of perceived divergence seemed to depend on instantaneous g level. This perceptual observation suggested a vertical misalignment of the eyes (vertical skew), dependent on the magnitude of g level sensed by the otoliths. While performing a different experiment during parabolic flight we recorded binocular eye position and analyzed these data to corroborate the behavioral observations. Records were obtained from seven trials in five subjects, containing eye alignment in both 0 g and 1.8 g. The recordings confirm the presence of vertical skew that changed with g level. "Skew-differential" was quantified for each trial as the difference in vertical skew from 0 g to 1.8 g. Mean skew-differential was 1.37°; the largest was 2.57°. Statistical significance was assessed using the student t-test and the more correct and stringent Generalized Estimating Equations (GEE). The observed skew is equivalent to a mild strabismus, which is known to result in diplopia. The underlying mechanism may be an asymmetry between the otolith organs on either side, which is centrally compensated in 1 g, but is inappropriately compensated in other gravitational fields. If equivalent amounts of vertical skew were to occur during changes in g level during dynamic phases of flight in high-performance aircraft or space shuttle reentry, the impact on visual fixation might be detrimental to piloting performance.

Changes in the perceived head transversal plane and the subjective visual horizontal induced by Coriolis stimulation during gondola centrifugation

For studying the influence of the vertical semicircular canals on spatial orientation in roll, the subjective visual horizontal (SVH) and the subjective transversal plane of the head (STP) were measured in a situation where the vertical canals sense a roll-velocity stimulus while the otolith organs persistently signal that the head is upright in roll. During gondola centrifugation (resultant gravitoinertial force vector 2.5 G, gondola inclination 66 degrees) subjects were exposed to controlled rotational head movements (angular speed 27 degrees/s, magnitude 40 degrees) about the yaw (body z-) axis, produced by means of a motor-driven helmet. This causes a roll-plane Coriolis stimulus to the canals, while the otoliths persistently sense upright head position in roll. The subjects reported intense sensations of rotation and tilt in the roll plane. This was reflected in tilts of both the SVH and STP. The initial tilt of the SVH was 13.0 ± 9.7 degrees (mean ± S.D., n=10). {The STP was changed in the opposite direction}. The initial tilt was 23.8 ± 12.2 degrees (mean ± S.D., n=5). {The changes in the SVH and STP were not of equal magnitude.} A few subjects who had almost no deviations in the SVH showed pronounced tilts of the STP. The time constant for exponential decay of the tilts of the SVH and STP was on average approximately 1 minute. These findings indicate that a difference in activity of the vertical canals in the right versus left ear may cause substantial tilts of the SVH even if there is no asymmetry in the activity of the otolith system. Further, the canal stimulus may induce a tilt of the fundamental egocentric frame of reference.

Context-specific adaptation of saccade gain in parabolic flight

Previous studies established that vestibular reflexes can have two adapted states (e.g., gains) simultaneously, and that a context cue (e.g., vertical eye position) can switch between the two states. Our earlier work demonstrated this phenomenon of context-specific adaptation for saccadic eye movements: we asked for gain decrease in one context state and gain increase in another context state, and then determined if a change in the context state would invoke switching between the adapted states. Horizontal and vertical eye position and head orientation could serve, to varying degrees, as cues for switching between two different saccade gains. In the present study, we asked whether gravity magnitude could serve as a context cue: saccade adaptation was performed during parabolic flight, which provides alternating levels of gravitoinertial force (0 g and 1.8 g). Results were less robust than those from ground experiments, but established that different saccade magnitudes could be associated with different gravity levels.

Neural Processing of Gravitoinertial Cues in Humans. III. Modeling Tilt and Translation Responses

All linear accelerometers measure gravitoinertial force, which is the sum of gravitational force (tilt) and inertial force due to linear acceleration (translation). Neural strategies must exist to elicit tilt and translation responses from this ambiguous cue. To investigate these neural processes, we developed a model of human responses and simulated a number of motion paradigms used to investigate this tilt/translation ambiguity. In this model, the separation of GIF into neural estimates of gravity and linear acceleration is accomplished via an internal model made up of three principal components: 1) the influence of rotational cues (e.g., semicircular canals) on the neural representation of gravity, 2) the resolution of gravitoinertial force into neural representations of gravity and linear acceleration, and 3) the neural representation of the dynamics of the semicircular canals. By combining these simple hypotheses within the internal model framework, the model mimics human responses to a number of different paradigms, ranging from simple paradigms, like roll tilt, to complex paradigms, like postrotational tilt and centrifugation. It is important to note that the exact same mechanisms can explain responses induced by simple movements as well as by more complex paradigms; no additional elements or hypotheses are needed to match the data obtained during more complex paradigms. Therefore these modeled response characteristics are consistent with available data and with the hypothesis that the nervous system uses internal models to estimate tilt and translation in the presence of ambiguous sensory cues.