Joseph McIntyre

Does the brain model Newton's laws?

How does the nervous system synchronize movements to catch a falling ball? According to one theory, only sensory information is used to estimate time-to-contact (TTC) with an approaching object; alternatively, implicit knowledge about physics may come into play. Here we show that astronauts initiated catching movements earlier in 0 g than in 1 g, which demonstrates that the brain uses an internal model of gravity to supplement sensory information when estimating TTC.

Visuo-motor coordination and internal models for object interception

Intercepting and avoiding collisions with moving objects are fundamental skills in daily life. Anticipatory behavior is required because of significant delays in transforming sensory information about target and body motion into a timed motor response. The ability to predict the kinematics and kinetics of interception or avoidance hundreds of milliseconds before the event may depend on several different sources of information and on different strategies of sensory-motor coordination. What are exactly the sources of spatio-temporal information and what are the control strategies remain controversial issues. Indeed, these topics have been the battlefield of contrasting views on how the brain interprets visual information to guide movement. Here we attempt a synthetic overview of the vast literature on interception. We discuss in detail the behavioral and neurophysiological aspects of interception of targets falling under gravity, as this topic has received special attention in recent years. We show that visual cues alone are insufficient to predict the time and place of interception or avoidance, and they need to be supplemented by prior knowledge (or internal models) about several features of the dynamic interaction with the moving object.

KINEMATIC AND DYNAMIC PROCESSES FOR THE CONTROL OF POINTING MOVEMENTS IN HUMANS REVEALED BY SHORT-TERM EXPOSURE TO MICROGRAVITY

The generation of accurate motor commands requires implicit knowledge of both limb and environmental dynamics. The action of gravity on moving limb segments must be taken into account within the motor command, and may affect the limb trajectory chosen to accomplish a given motor task. Exactly how the CNS deals with these gravitoinertial forces remains an open question. Does the CNS measure gravitational forces directly, or are they accommodated in the motor plan by way of internal models of physical laws? In this study five male subjects participated. We measured kinematic and dynamic parameters of upward and downward arm movements executed at two different speeds, in both normal Earth gravity and in the weightless conditions of parabolic flight. Exposure to microgravity affected velocity profiles for both directions and speeds. The shape of velocity profiles (the ratio of maximum to mean velocity) and movement duration both showed transient perturbations initially in microgravity, but returned to normal gravity values with practice in 0 x g. Differences in relative time to peak velocity between upward versus downward movements, persisted for all trial performed in weightlessness. These differences in kinematic profiles and in the torque profiles used to produce them, diminished, however, with practice in 0 x g. These findings lead to the conclusion that the CNS explicitly represents gravitational and inertial forces in the internal models used to generate and execute arm movements. Furthermore, the results suggest that the CNS adapts motor plans to novel environments on different time scales; dynamics adapt first to reproduce standard kinematics, and then kinematics patterns are adapted to optimize dynamics.

Viewer-centered and body-centered frames of reference in direct visuomotor transformations

Abstract It has been hypothesized that the end-point position of reaching may be specified in an egocentric frame of reference. In most previous studies, however, reaching was toward a memorized target, rather than an actual target. Thus, the role played by sensorimotor transformation could not be disassociated from the role played by storage in short-term memory. In the present study the direct process of sensorimotor transformation was investigated in reaching toward continuously visible targets that need not be stored in memory. A virtual reality system was used to present visual targets in different three-dimensional (3D) locations in two different tasks, one with visual feedback of the hand and arm position (Seen Hand) and the other without such feedback (Unseen Hand). In the Seen Hand task, the axes of maximum variability and of maximum contraction converge toward the mid-point between the eyes. In the Unseen Hand task only the maximum contraction correlates with the sight-line and the axes of maximum variability are not viewer-centered but rotate anti-clockwise around the body and the effector arm during the move from the right to the left workspace. The bulk of findings from these and previous experiments support the hypothesis of a two-stage process, with a gradual transformation from viewer-centered to body-centered and arm-centered coordinates. Retinal, extra-retinal and arm-related signals appear to be progressively combined in superior and inferior parietal areas, giving rise to egocentric representations of the end-point position of reaching.

Hand trajectories of vertical arm movements in one-G and zero-G environments. Evidence for a central representation of gravitational force.

Abstract The purpose of the present experiment was to study the way in which the central nervous system (CNS), represents gravitational force during vertical arm pointing movements. Movements in upward (against gravity) and downward (with gravity) directions, with two different mass loads (hand empty and with a hand-held 0.5-kg weight) were executed by eight subjects in a normal gravitational environment. Movements by two cosmonauts, in the two directions, were also tested in a state of weightlessness. Analyses focused upon finger trajectories in the saggital plane. Subjects in a normal gravitational environment showed curved paths for both directions and weight conditions. In addition, downward movements showed significantly smaller curvatures than upward movements. Movement times were approximately the same for all the experimental conditions. Curvature differences between upward and downward movements persisted during space flight and immediately postflight. Movement times from both cosmonauts increased slightly during flight, but returned to normal immediately on reentry in a one-G environment. Results from the present study provide evidence that gravity is centrally represented in an anticipatory fashion as a driving force during vertical arm movement planning.

Effect of gravity on human spontaneous 10-Hz electroencephalographic oscillations during the arrest reaction.

Electroencephalographic oscillations at 10 Hz (alpha and mu rhythms) are the most prominent rhythms observed in awake, relaxed (eye-closed) subjects. These oscillations may be considered as a marker of cortical inactivity or an index of the active inhibition of the sensory information. Different cortical sources may participate in the 10-Hz oscillation and appear to be modulated by the sensory context and functional demands. In microgravity, the marked reduction in multimodal graviceptive inputs to cortical networks participating in the representation of space could be expected to affect the 10-Hz activity. The effect of microgravity on this basic oscillation has heretofore not been studied quantitatively. Because the alpha rhythm has a functional role in the regulation of network properties of the visual areas, we hypothesised that the absence of gravity would affect its strength. Here, we report the results of an experiment conducted over the course of 3 space flights, in which we quantified the power of the 10-Hz activity in relation to the arrest reaction (i.e., in 2 distinct physiological states: eyes open and eyes closed). We observed that the power of the spontaneous 10-Hz oscillation recorded in the eyes-closed state in the parieto-occipital (alpha rhythm) and sensorimotor areas (mu rhythm) increased in the absence of gravity. The suppression coefficient during the arrest reaction and the related spectral perturbations produced by eye-opening/closure state transition also increased in on orbit. These results are discussed in terms of current theories on the source and the importance of the alpha rhythm for cognitive function.

Reference frames and internal models for visuo-manual coordination: what can we learn from microgravity experiments?

Gravity plays a role in many different levels of human motor behavior. It dictates the laws of motion of our body and limbs, as well as of the objects in the external world with which we wish to interact. The dynamic interaction of our body with the world is molded within gravitys constraints. The task of catching a ball that has been thrown toward a human subject typifies the kind of constraints that the nervous system must take into consideration during visuo-manual coordination on earth. By dissecting and examining the components of this task, one can see what kinds of problems must be solved by the central nervous system to generate coordinated motor actions in response to incoming sensory information. In this review, we use the example of a ball catching task to outline various issues in the field of human motor control and to ask the question as to how the microgravity environment of lower earth orbit can be used to probe the functioning of the human motor system.

Gravity affects the preferred vertical and horizontal in visual perception of orientation

The aim of this study was to evaluate the influence of gravity on the representation and storage of visual orientation information. On earth, measurements of response time and variability for a task of aligning remembered visual stimuli showed a distinct preference for horizontally and vertically oriented stimuli when the body and gravitational axes were aligned. This preference was markedly decreased or disappeared when the body axis was tilted with respect to gravity but was maintained for tests performed in microgravity. We conclude that subjects acquire and store visual orientation in a multi-modal reference frame that combines proprioceptive and gravitational information when both are available.

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 balls 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 targets most likely acceleration. Here we used the peculiar conditions of parabolic flight—where gravitys 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 gravitys pull plays a role in coordinating quick reactions intended to intercept a fast-moving visual target.

Movement Stability Under Uncertain Internal Models of Dynamics

Sensory noise and feedback delay are potential sources of instability and variability for the on-line control of movement. It is commonly assumed that predictions based on internal models allow the CNS to anticipate the consequences of motor actions and protect the movements from uncertainty and instability. However, during motor learning and exposure to unknown dynamics, these predictions can be inaccurate. Therefore a distinct strategy is necessary to preserve movement stability. This study tests the hypothesis that in such situations, subjects adapt the speed and accuracy constraints on the movement, yielding a control policy that is less prone to undesirable variability in the outcome. This hypothesis was tested by asking subjects to hold a manipulandum in precision grip and to perform single-joint, discrete arm rotations during short-term exposure to weightlessness (0 g), where the internal models of the limb dynamics must be updated. Measurements of grip force adjustments indicated that the internal predictions were altered during early exposure to the 0 g condition. Indeed, the grip force/load force coupling reflected that the grip force was less finely tuned to the load-force variations at the beginning of the exposure to the novel gravitational condition. During this learning period, movements were slower with asymmetric velocity profiles and target undershooting. This effect was compared with theoretical results obtained in the context of optimal feedback control, where changing the movement objective can be directly tested by adjusting the cost parameters. The effect on the simulated movements quantitatively supported the hypothesis of a change in cost function during early exposure to a novel environment. The modified optimization criterion reduces the trial-to-trial variability in spite of the fact that noise affects the internal prediction. These observations support the idea that the CNS adjusts the movement objective to stabilize the movement when internal models are uncertain.