Body orientation contributes to modelling the effects of gravity for target interception in humans.

KEY POINTS: It is known that interception of targets accelerated by gravity involves internal models coupled with visual signals. Non-visual signals related to head and body orientation relative to gravity may also contribute, although their role is poorly understood. In a novel experiment, we asked pitched observers to hit a virtual target approaching with an acceleration that was either coherent or incoherent with their pitch-tilt. Initially, the timing errors were large and independent of the coherence between target acceleration and observer's pitch. With practice, however, the timing errors became substantially smaller in the coherent conditions. The results show that information about head and body orientation can contribute to modelling the effects of gravity on a moving target. Orientation cues from vestibular and somatosensory signals might be integrated with visual signals in the vestibular cortex, where the internal model of gravity is assumed to be encoded. ABSTRACT: Interception of moving targets relies on visual signals and internal models. Less is known about the additional contribution of non-visual cues about head and body orientation relative to gravity. We took advantage of Galileo's law of motion along an incline to demonstrate the effects of vestibular and somatosensory cues about head and body orientation on interception timing. Participants were asked to hit a ball rolling in a gutter towards the eyes, resulting in image expansion. The scene was presented in a head-mounted display, without any visual information about gravity direction. In separate blocks of trials participants were pitched backwards by 20° or 60°, whereas ball acceleration was randomized across trials so as to be compatible with rolling down a slope of 20° or 60°. Initially, the timing errors were large, independently of the coherence between ball acceleration and pitch angle, consistent with responses based exclusively on visual information because visual stimuli were identical at both tilts. At the end of the experiment, however, the timing errors were systematically smaller in the coherent conditions than the incoherent ones. Moreover, the responses were significantly (P = 0.007) earlier when participants were pitched by 60° than when they were pitched by 20°. Therefore, practice with the task led to incorporation of information about head and body orientation relative to gravity for response timing. Instead, posture did not affect response timing in a control experiment in which participants hit a static target in synchrony with the last of a predictable series of stationary audiovisual stimuli.

Motion direction, luminance contrast, and speed perception: An unexpected meeting.

Motion direction and luminance contrast are two central features in the representation of visual motion in humans. In five psychophysical experiments, we showed that these two features affect the perceived speed of a visual stimulus. Our data showed a surprising interaction between contrast and direction. Participants perceived downward moving stimuli as faster than upward or rightward stimuli, but only at high contrast. Likewise, luminance contrast produced an underestimation of motion speed, but mostly when the stimuli moved downward. We explained these novel phenomena by means of a theoretical model, accounting for prior knowledge of motion dynamics.

The speed-curvature power law of movements: a reappraisal.

Several types of curvilinear movements obey approximately the so called 2/3 power law, according to which the angular speed varies proportionally to the 2/3 power of the curvature. The origin of the law is debated but it is generally thought to depend on physiological mechanisms. However, a recent paper (Marken and Shaffer, Exp Brain Res 88:685-690, 2017) claims that this power law is simply a statistical artifact, being a mathematical consequence of the way speed and curvature are calculated. Here we reject this hypothesis by showing that the speed-curvature power law of biological movements is non-trivial. First, we confirm that the power exponent varies with the shape of human drawing movements and with environmental factors. Second, we report experimental data from Drosophila larvae demonstrating that the power law does not depend on how curvature is calculated. Third, we prove that the law can be violated by means of several mathematical and physical examples. Finally, we discuss biological constraints that may underlie speed-curvature power laws discovered in empirical studies.

Intercepting virtual balls approaching under different gravity conditions: evidence for spatial prediction.

To accurately time motor responses when intercepting falling balls we rely on an internal model of gravity. However, whether and how such a model is also used to estimate the spatial location of interception is still an open question. Here we addressed this issue by asking 25 participants to intercept balls projected from a fixed location 6 m in front of them and approaching along trajectories with different arrival locations, flight durations, and gravity accelerations (0g and 1g). The trajectories were displayed in an immersive virtual reality system with a wide field of view. Participants intercepted approaching balls with a racket, and they were free to choose the time and place of interception. We found that participants often achieved a better performance with 1g than 0g balls. Moreover, the interception points were distributed along the direction of a 1g path for both 1g and 0g balls. In the latter case, interceptions tended to cluster on the upper half of the racket, indicating that participants aimed at a lower position than the actual 0g path. These results suggest that an internal model of gravity was probably used in predicting the interception locations. However, we found that the difference in performance between 1g and 0g balls was modulated by flight duration, the difference being larger for faster balls. In addition, the number of peaks in the hand speed profiles increased with flight duration, suggesting that visual information was used to adjust the motor response, correcting the prediction to some extent.NEW & NOTEWORTHY Here we show that an internal model of gravity plays a key role in predicting where to intercept a fast-moving target. Participants also assumed an accelerated motion when intercepting balls approaching in a virtual environment at constant velocity. We also show that the role of visual information in guiding interceptive movement increases when more time is available.

The speed-curvature power law in Drosophila larval locomotion.

We report the discovery that the locomotor trajectories of Drosophila larvae follow the power-law relationship between speed and curvature previously found in the movements of human and non-human primates. Using high-resolution behavioural tracking in controlled but naturalistic sensory environments, we tested the law in maggots tracing different trajectory types, from reaching-like movements to scribbles. For most but not all flies, we found that the law holds robustly, with an exponent close to three-quarters rather than to the usual two-thirds found in almost all human situations, suggesting dynamic effects adding on purely kinematic constraints. There are different hypotheses for the origin of the law in primates, one invoking cortical computations, another viscoelastic muscle properties coupled with central pattern generators. Our findings are consistent with the latter view and demonstrate that the law is possible in animals with nervous systems orders of magnitude simpler than in primates. Scaling laws might exist because natural selection favours processes that remain behaviourally efficient across a wide range of neural and body architectures in distantly related species.

Hand interception of occluded motion in humans: a test of model-based vs. on-line control.

Two control schemes have been hypothesized for the manual interception of fast visual targets. In the model-free on-line control, extrapolation of target motion is based on continuous visual information, without resorting to physical models. In the model-based control, instead, a prior model of target motion predicts the future spatiotemporal trajectory. To distinguish between the two hypotheses in the case of projectile motion, we asked participants to hit a ball that rolled down an incline at 0.2 g and then fell in air at 1 g along a parabola. By varying starting position, ball velocity and trajectory differed between trials. Motion on the incline was always visible, whereas parabolic motion was either visible or occluded. We found that participants were equally successful at hitting the falling ball in both visible and occluded conditions. Moreover, in different trials the intersection points were distributed along the parabolic trajectories of the ball, indicating that subjects were able to extrapolate an extended segment of the target trajectory. Remarkably, this trend was observed even at the very first repetition of movements. These results are consistent with the hypothesis of model-based control, but not with on-line control. Indeed, ball path and speed during the occlusion could not be extrapolated solely from the kinematic information obtained during the preceding visible phase. The only way to extrapolate ball motion correctly during the occlusion was to assume that the ball would fall under gravity and air drag when hidden from view. Such an assumption had to be derived from prior experience.

Familiar trajectories facilitate the interpretation of physical forces when intercepting a moving target.

Familiarity with the visual environment affects our expectations about the objects in a scene, aiding in recognition and interaction. Here we tested whether the familiarity with the specific trajectory followed by a moving target facilitates the interpretation of the effects of underlying physical forces. Participants intercepted a target sliding down either an inclined plane or a tautochrone. Gravity accelerated the target by the same amount in both cases, but the inclined plane represented a familiar trajectory whereas the tautochrone was unfamiliar to the participants. In separate sessions, the gravity field was consistent with either natural gravity or artificial reversed gravity. Target motion was occluded from view over the last segment. We found that the responses in the session with unnatural forces were systematically delayed relative to those with natural forces, but only for the inclined plane. The time shift is consistent with a bias for natural gravity, in so far as it reflects an a priori expectation that a target not affected by natural forces will arrive later than one accelerated downwards by gravity. Instead, we did not find any significant time shift with unnatural forces in the case of the tautochrone. We argue that interception of a moving target relies on the integration of the high-level cue of trajectory familiarity with low-level cues related to target kinematics.

When up is down in 0g: how gravity sensing affects the timing of interceptive actions.

Humans are known to regulate the timing of interceptive actions by modeling, in a simplified way, Newtonian mechanics. Specifically, when intercepting an approaching ball, humans trigger their movements a bit earlier when the target arrives from above than from below. This bias occurs regardless of the ball's true kinetics, and thus appears to reflect an a priori expectation that a downward moving object will accelerate. We postulate that gravito-inertial information is used to tune visuomotor responses to match the target's most likely acceleration. Here we used the peculiar conditions of parabolic flight--where gravity's effects change every 20 s--to test this hypothesis. We found a striking reversal in the timing of interceptive responses performed in weightlessness compared with trials performed on ground, indicating a role of gravity sensing in the tuning of this response. Parallels between these observations and the properties of otolith receptors suggest that vestibular signals themselves might plausibly provide the critical input. Thus, in addition to its acknowledged importance for postural control, gaze stabilization, and spatial navigation, we propose that detecting the direction of gravity's pull plays a role in coordinating quick reactions intended to intercept a fast-moving visual target.

Enhancement of Vestibular Motion Discrimination by Small Stochastic Whole-body Perturbations in Young Healthy Humans.

Noisy galvanic vestibular stimulation has been shown to improve vestibular perception in healthy subjects. Here, we sought to obtain similar results using more natural stimuli consisting of small-amplitude motion perturbations of the whole body. Thirty participants were asked to report the perceived direction of antero-posterior sinusoidal motion on a MOOG platform. We compared the baseline perceptual thresholds with those obtained by applying small, stochastic perturbations at different power levels along the antero-posterior axis, symmetrically distributed around a zero-mean. At the population level, we found that the thresholds for all but the highest level of noise were significantly lower than the baseline threshold. At the individual level, the threshold was lower with at least one noise level than the threshold without noise in 87% of participants. Thus, small, stochastic oscillations of the whole body can increase the probability of recognizing the direction of motion from low, normally subthreshold vestibular signals, possibly due to stochastic resonance mechanisms. We suggest that, just as the external noise of the present experiments, also the spontaneous random oscillations of the head and body associated with standing posture are beneficial by enhancing vestibular thresholds with a mechanism similar to stochastic resonance.

Noise and vestibular perception of passive self-motion.

Noise defined as random disturbances is ubiquitous in both the external environment and the nervous system. Depending on the context, noise can degrade or improve information processing and performance. In all cases, it contributes to neural systems dynamics. We review some effects of various sources of noise on the neural processing of self-motion signals at different stages of the vestibular pathways and the resulting perceptual responses. Hair cells in the inner ear reduce the impact of noise by means of mechanical and neural filtering. Hair cells synapse on regular and irregular afferents. Variability of discharge (noise) is low in regular afferents and high in irregular units. The high variability of irregular units provides information about the envelope of naturalistic head motion stimuli. A subset of neurons in the vestibular nuclei and thalamus are optimally tuned to noisy motion stimuli that reproduce the statistics of naturalistic head movements. In the thalamus, variability of neural discharge increases with increasing motion amplitude but saturates at high amplitudes, accounting for behavioral violation of Weber's law. In general, the precision of individual vestibular neurons in encoding head motion is worse than the perceptual precision measured behaviorally. However, the global precision predicted by neural population codes matches the high behavioral precision. The latter is estimated by means of psychometric functions for detection or discrimination of whole-body displacements. Vestibular motion thresholds (inverse of precision) reflect the contribution of intrinsic and extrinsic noise to perception. Vestibular motion thresholds tend to deteriorate progressively after the age of 40 years, possibly due to oxidative stress resulting from high discharge rates and metabolic loads of vestibular afferents. In the elderly, vestibular thresholds correlate with postural stability: the higher the threshold, the greater is the postural imbalance and risk of falling. Experimental application of optimal levels of either galvanic noise or whole-body oscillations can ameliorate vestibular function with a mechanism reminiscent of stochastic resonance. Assessment of vestibular thresholds is diagnostic in several types of vestibulopathies, and vestibular stimulation might be useful in vestibular rehabilitation.

Head-centric computing for vestibular stimulation under head-free conditions.

Background: The vestibular end organs (semicircular canals, saccule and utricle) monitor head orientation and motion. Vestibular stimulation by means of controlled translations, rotations or tilts of the head represents a routine manoeuvre to test the vestibular apparatus in a laboratory or clinical setting. In diagnostics, it is used to assess oculomotor postural or perceptual responses, whose abnormalities can reveal subclinical vestibular dysfunctions due to pathology, aging or drugs. Objective: The assessment of the vestibular function requires the alignment of the motion stimuli as close as possible with reference axes of the head, for instance the cardinal axes naso-occipital, interaural, cranio-caudal. This is often achieved by using a head restraint, such as a helmet or strap holding the head tightly in a predefined posture that guarantees the alignment described above. However, such restraints may be quite uncomfortable, especially for elderly or claustrophobic patients. Moreover, it might be desirable to test the vestibular function under the more natural conditions in which the head is free to move, as when subjects are tracking a visual target or they are standing erect on the moving platform. Here, we document algorithms that allow delivering motion stimuli aligned with head-fixed axes under head-free conditions. Methods: We implemented and validated these algorithms using a MOOG-6DOF motion platform in two different conditions. 1) The participant kept the head in a resting, fully unrestrained posture, while inter-aural, naso-occipital or cranio-caudal translations were applied. 2) The participant moved the head continuously while a naso-occipital translation was applied. Head and platform motion were monitored in real-time using Vicon. Results: The results for both conditions showed excellent agreement between the theoretical spatio-temporal profile of the motion stimuli and the corresponding profile of actual motion as measured in real-time. Conclusion: We propose our approach as a safe, non-intrusive method to test the vestibular system under the natural head-free conditions required by the experiential perspective of the patients.

Patterned control of human locomotion.

There is much experimental evidence for the existence of biomechanical constraints which simplify the problem of control of multi-segment movements. In addition, it has been hypothesized that movements are controlled using a small set of basic temporal components or activation patterns, shared by several different muscles and reflecting global kinematic and kinetic goals. Here we review recent studies on human locomotion showing that muscle activity is accounted for by a combination of few basic patterns, each one timed at a different phase of the gait cycle. Similar patterns are involved in walking and running at different speeds, walking forwards or backwards, and walking under different loading conditions. The corresponding weights of distribution to different muscles may change as a function of the condition, allowing highly flexible control. Biomechanical correlates of each activation pattern have been described, leading to the hypothesis that the co-ordination of limb and body segments arises from the coupling of neural oscillators between each other and with limb mechanical oscillators. Muscle activations need only intervene during limited time epochs to force intrinsic oscillations of the system when energy is lost.

Observing human movements helps decoding environmental forces.

Vision of human actions can affect several features of visual motion processing, as well as the motor responses of the observer. Here, we tested the hypothesis that action observation helps decoding environmental forces during the interception of a decelerating target within a brief time window, a task intrinsically very difficult. We employed a factorial design to evaluate the effects of scene orientation (normal or inverted) and target gravity (normal or inverted). Button-press triggered the motion of a bullet, a piston, or a human arm. We found that the timing errors were smaller for upright scenes irrespective of gravity direction in the Bullet group, while the errors were smaller for the standard condition of normal scene and gravity in the Piston group. In the Arm group, instead, performance was better when the directions of scene and target gravity were concordant, irrespective of whether both were upright or inverted. These results suggest that the default viewer-centered reference frame is used with inanimate scenes, such as those of the Bullet and Piston protocols. Instead, the presence of biological movements in animate scenes (as in the Arm protocol) may help processing target kinematics under the ecological conditions of coherence between scene and target gravity directions.

Coherence of structural visual cues and pictorial gravity paves the way for interceptive actions.

Dealing with upside-down objects is difficult and takes time. Among the cues that are critical for defining object orientation, the visible influence of gravity on the object's motion has received limited attention. Here, we manipulated the alignment of visible gravity and structural visual cues between each other and relative to the orientation of the observer and physical gravity. Participants pressed a button triggering a hitter to intercept a target accelerated by a virtual gravity. A factorial design assessed the effects of scene orientation (normal or inverted) and target gravity (normal or inverted). We found that interception was significantly more successful when scene direction was concordant with target gravity direction, irrespective of whether both were upright or inverted. This was so independent of the hitter type and when performance feedback to the participants was either available (Experiment 1) or unavailable (Experiment 2). These results show that the combined influence of visible gravity and structural visual cues can outweigh both physical gravity and viewer-centered cues, leading to rely instead on the congruence of the apparent physical forces acting on people and objects in the scene.

Mental imagery of object motion in weightlessness.

Mental imagery represents a potential countermeasure for sensorimotor and cognitive dysfunctions due to spaceflight. It might help train people to deal with conditions unique to spaceflight. Thus, dynamic interactions with the inertial motion of weightless objects are only experienced in weightlessness but can be simulated on Earth using mental imagery. Such training might overcome the problem of calibrating fine-grained hand forces and estimating the spatiotemporal parameters of the resulting object motion. Here, a group of astronauts grasped an imaginary ball, threw it against the ceiling or the front wall, and caught it after the bounce, during pre-flight, in-flight, and post-flight experiments. They varied the throwing speed across trials and imagined that the ball moved under Earth's gravity or weightlessness. We found that the astronauts were able to reproduce qualitative differences between inertial and gravitational motion already on ground, and further adapted their behavior during spaceflight. Thus, they adjusted the throwing speed and the catching time, equivalent to the duration of virtual ball motion, as a function of the imaginary 0 g condition versus the imaginary 1 g condition. Arm kinematics of the frontal throws further revealed a differential processing of imagined gravity level in terms of the spatial features of the arm and virtual ball trajectories. We suggest that protocols of this kind may facilitate sensorimotor adaptation and help tuning vestibular plasticity in-flight, since mental imagery of gravitational motion is known to engage the vestibular cortex.

Watching the Effects of Gravity. Vestibular Cortex and the Neural Representation of "Visual" Gravity.

Gravity is a physical constraint all terrestrial species have adapted to through evolution. Indeed, gravity effects are taken into account in many forms of interaction with the environment, from the seemingly simple task of maintaining balance to the complex motor skills performed by athletes and dancers. Graviceptors, primarily located in the vestibular otolith organs, feed the Central Nervous System with information related to the gravity acceleration vector. This information is integrated with signals from semicircular canals, vision, and proprioception in an ensemble of interconnected brain areas, including the vestibular nuclei, cerebellum, thalamus, insula, retroinsula, parietal operculum, and temporo-parietal junction, in the so-called vestibular network. Classical views consider this stage of multisensory integration as instrumental to sort out conflicting and/or ambiguous information from the incoming sensory signals. However, there is compelling evidence that it also contributes to an internal representation of gravity effects based on prior experience with the environment. This a priori knowledge could be engaged by various types of information, including sensory signals like the visual ones, which lack a direct correspondence with physical gravity. Indeed, the retinal accelerations elicited by gravitational motion in a visual scene are not invariant, but scale with viewing distance. Moreover, the "visual" gravity vector may not be aligned with physical gravity, as when we watch a scene on a tilted monitor or in weightlessness. This review will discuss experimental evidence from behavioral, neuroimaging (connectomics, fMRI, TMS), and patients' studies, supporting the idea that the internal model estimating the effects of gravity on visual objects is constructed by transforming the vestibular estimates of physical gravity, which are computed in the brainstem and cerebellum, into internalized estimates of virtual gravity, stored in the vestibular cortex. The integration of the internal model of gravity with visual and non-visual signals would take place at multiple levels in the cortex and might involve recurrent connections between early visual areas engaged in the analysis of spatio-temporal features of the visual stimuli and higher visual areas in temporo-parietal-insular regions.

Perceptual judgments of duration of parabolic motions.

In a 2-alternative forced-choice protocol, observers judged the duration of ball motions shown on an immersive virtual-reality display as approaching in the sagittal plane along parabolic trajectories compatible with Earth gravity effects. In different trials, the ball shifted along the parabolas with one of three different laws of motion: constant tangential velocity, constant vertical velocity, or gravitational acceleration. Only the latter motion was fully consistent with Newton's laws in the Earth gravitational field, whereas the motions with constant velocity profiles obeyed the spatio-temporal constraint of parabolic paths dictated by gravity but violated the kinematic constraints. We found that the discrimination of duration was accurate and precise for all types of motions, but the discrimination for the trajectories at constant tangential velocity was slightly but significantly more precise than that for the trajectories at gravitational acceleration or constant vertical velocity. The results are compatible with a heuristic internal representation of gravity effects that can be engaged when viewing projectiles shifting along parabolic paths compatible with Earth gravity, irrespective of the specific kinematics. Opportunistic use of a moving frame attached to the target may favour visual tracking of targets with constant tangential velocity, accounting for the slightly superior duration discrimination.

Extrapolation of vertical target motion through a brief visual occlusion.

It is known that arbitrary target accelerations along the horizontal generally are extrapolated much less accurately than target speed through a visual occlusion. The extent to which vertical accelerations can be extrapolated through an occlusion is much less understood. Here, we presented a virtual target rapidly descending on a blank screen with different motion laws. The target accelerated under gravity (1g), decelerated under reversed gravity (-1g), or moved at constant speed (0g). Probability of each type of acceleration differed across experiments: one acceleration at a time, or two to three different accelerations randomly intermingled could be presented. After a given viewing period, the target disappeared for a brief, variable period until arrival (occluded trials) or it remained visible throughout (visible trials). Subjects were asked to press a button when the target arrived at destination. We found that, in visible trials, the average performance with 1g targets could be better or worse than that with 0g targets depending on the acceleration probability, and both were always superior to the performance with -1g targets. By contrast, the average performance with 1g targets was always superior to that with 0g and -1g targets in occluded trials. Moreover, the response times of 1g trials tended to approach the ideal value with practice in occluded protocols. To gain insight into the mechanisms of extrapolation, we modeled the response timing based on different types of threshold models. We found that occlusion was accompanied by an adaptation of model parameters (threshold time and central processing time) in a direction that suggests a strategy oriented to the interception of 1g targets at the expense of the interception of the other types of tested targets. We argue that the prediction of occluded vertical motion may incorporate an expectation of gravity effects.