Ashton Graybiel Spatial Orientation Laboratory, Brandeis University, Waltham, Massachusetts 02254-9110
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ABSTRACT |
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Lackner, James R. and Paul DiZio. Gravitoinertial force background level affects adaptation to Coriolis force perturbations of reaching movements. J. Neurophysiol. 80: 546-553, 1998. We evaluated the combined effects on reaching movements of the transient, movement-dependent Coriolis forces and the static centrifugal forces generated in a rotating environment. Specifically, we assessed the effects of comparable Coriolis force perturbations in different static force backgrounds. Two groups of subjects made reaching movements toward a just-extinguished visual target before rotation began, during 10 rpm counterclockwise rotation, and after rotation ceased. One group was seated on the axis of rotation, the other 2.23 m away. The resultant of gravity and centrifugal force on the hand was 1.0 g for the on-center group during 10 rpm rotation, and 1.031 g for the off-center group because of the 0.25 g centrifugal force present. For both groups, rightward Coriolis forces, 0.2 g peak, were generated during voluntary arm movements. The endpoints and paths of the initial per-rotation movements were deviated rightward for both groups by comparable amounts. Within 10 subsequent reaches, the on-center group regained baseline accuracy and straight-line paths; however, even after 40 movements the off-center group had not resumed baseline endpoint accuracy. Mirror-image aftereffects occurred when rotation stopped. These findings demonstrate that manual control is disrupted by transient Coriolis force perturbations and that adaptation can occur even in the absence of visual feedback. An increase, even a small one, in background force level above normal gravity does not affect the size of the reaching errors induced by Coriolis forces nor does it affect the rate of reacquiring straight reaching paths; however, it does hinder restoration of reaching accuracy.
Rotating a space craft to generate artificial gravity is a potential way of preventing cardiac deconditioning, muscle atrophy, skeletal structural changes, and of enhancing hygiene and livability during interplanetary missions. In a rotating space vehicle, artificial gravity is actually the centrifugal force (Fcent) associated with rotation and is proportional to
Subjects
Twenty individuals participated. They were without vestibular or sensory-motor impairments that could have influenced their performance and had normal or corrected to normal vision.
Apparatus
A test chair that could be relocated in the rotating room was used for both test conditions. The chair had a head holder that was adjusted for individual subjects to comfortably support the head and prevent significant movements. A horizontal Plexiglas surface was fixed to the chair at waist level with a light-emitting diode (LED) embedded in its surface from below serving as a target. During testing, the LED was the only object ever visible because the room lights were turned off. The LED remained illuminated only so long as the subject depressed a microswitch that marked the start position; when the finger was lifted to point to the LED it went out. The LED was located 35 cm in front of the microswitch, and both were ~25 cm right of the subject's midline. The surface of the Plexiglas was perfectly smooth so that the subject could not receive tactile cues about the LED's position. Reaching movements to the target were recorded by a WATSMART motion monitoring system that tracked an infrared emitter taped to the subject's right index finger.
Procedure
Ten subjects were tested seated at the center of rotation; the chair was located so that the start button was directly on the rotation axis of the SRR (see Fig. 1). The other 10 were tested 2.23 m away facing the center of rotation. The centrifugal force generated by rotation and thus the resultant force on the hand depended on arm position. On center, with the arm in the start position, the centrifugal force on the hand was zero (resultant gravitoinertial force equal to 1.0 g), with the arm extended 35 cm to place the finger on the target it was 0.04 g; this small force was directed forward assisting the movement. At 2.23 m from the center, with the arm in the start position, the centrifugal force on the hand was 0.25 g (resultant equal to 1.031 g), and with the finger on the target, it was 0.21 g, resisting the forward motion of the arm. In both conditions, a rightward, relative to the subject, Coriolis force was generated while the arm was moving.
Data analysis
Computer algorithms were used to identify the endpoint, duration, and peak forward velocity of each reaching movement. The endpoint and duration were defined as the position and time, respectively, at which the velocity of the finger first dropped to 5 mm/s. In addition, binary search algorithms were used to find the maximum leftward and rightward deviations of the finger from a straight line path between the start and endpoint, as a measure of trajectory curvature. Each subject's final 8 prerotation movements were averaged to obtain stable baseline performance measures. Endpoint and trajectory errors were obtained by computing differences from baseline. We computed both fore-aft endpoint errors (parallel to both the intended movement direction and the centrifugal forces, when present), and lateral endpoint errors (orthogonal to the intended movement direction and parallel to the Coriolis forces). Our a priori questions were whether G level affects 1) the size of reaching errors when Coriolis forces are first introduced (initial per-rotation reaches), 2) the extent of adaptive reduction in reaching errors that can be achieved by continued exposure to Coriolis forces in the two different static G backgrounds (final per-rotation reaches), and 3) the magnitude of aftereffect produced by persistence of adaptive compensations when Coriolis and centrifugal forces are again absent (initial postrotation reaches).
Prerotation, baseline reaches
Subjects in both force level groups made nearly straight reaches. The average endpoints fell 15 mm to the left of and 7 mm beyond the target for the on-center group, and 7 mm to the right and 6 mm beyond for the off-center group. The average movement trajectories were curved only 1 mm to the left for the on-center group and 1 mm to the right for the off-center group. These prerotation values of movement endpoint and trajectory curvature were statistically indistinguishable from the values for the final postrotation reaches, indicating that they represent a stable baseline for assessment of changes due to Coriolis forces, adaptation, and G level.
Reaching errors relative to baseline
A multivariate analysis of variance (Statistical Package for the Social Sciences MANOVA procedure) assessed whether reaching movements were affected by G level (1 g, on-center group and 1.031 g, off-center group; between subjects) and by the rotation exposure (initial per-rotation, final per-rotation, initial postrotation; within subjects). Lateral endpoints were affected by rotation [F(2,17) = 10.093, P = 0.001] and an interaction of rotation and G level [F(2,17) = 3.603, P = 0.049]. For curvature of movement trajectory there was only an effect of rotation [F(2,17) = 25.167, P < 0.0001]. Fore-aft endpoints showed no significant changes in the MANOVA. Figure 2 illustrates the average lateral and fore-aft endpoints and trajectory curvatures for the initial per-rotation, final per-rotation, and initial postrotation movements. The sections below describe the patterns observed during and after rotation and the results of our planned comparisons.
Per-rotation reaching errors
Subjects in both force backgrounds made large lateral errors but reached the correct distance in their first per-rotation movements. The movement trajectories were deflected rightward, in the direction of the Coriolis force (
Postrotation reaching errors
In their first postrotation reach, every subject in the on-center group showed lateral endpoint errors and trajectory deviations. These aftereffects were of equivalent magnitude but of opposite sign (i.e., they were mirror images) to their first per-rotation reaches. Lateral endpoint and trajectory values were significantly different both from prerotation baseline values and initial per-rotation values. With additional reaching movements, straight line trajectories and prerotation endpoints were regained within about a dozen movements.
Subjects tested in the rotating room at both force levels showed large lateral trajectory and endpoint deviations in their first reaching movements made at constant velocity rotation. The deviations were in the direction of the transient Coriolis forces generated by voluntary reaching movements. The initial trajectory and endpoint deviations are sufficiently large to be functionally significant in operating control panels and manipulating objects in a typical vehicle environment in space or on earth. These results are in accord with our earlier observations and constitute powerful evidence against equilibrium position theories of motor control, both the
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
2r where
is the rate of rotation and r the radius.1 Analyses of centrifugal and other forces in a rotating environment and predictions of their potential consequences for movement and object manipulation have been presented by several authors (Loret 1961; Nicogossian and McCormack 1987; Stone 1970
). Most adverse side effects of rotating environments reach their asymptotic minima at radii of ~40 m, which at 5 rpm would generate a 1-g artificial gravity level (Stone 1970
). Head movements made in a rotating environment, especially at high velocities of rotation, can be disorienting and nauseogenic (Graybiel et al. 1960
; Johnson et al. 1951
; Schubert 1932
). The reason for this is that making head movements about an axis other than that of rotation elicits a complex pattern of stimulation of the vestibular system known as Coriolis, cross-coupled stimulation. Graybiel and colleagues demonstrated that humans could adapt their head movement control relatively rapidly to rotation rates up to 5 rpm (Graybiel 1973
; Graybiel and Knepton 1972
; Graybiel and Wood 1969
). After adaptation, head movements again felt normal and no longer were disorienting or provocative. Other studies have shown that the nauseogenic and disorienting effects of Coriolis, cross-coupled stimulation depend on gravitoinertial force (G)2 background level, being enhanced at >1-g levels and diminished at <1-g acceleration (DiZio et al. 1987
; Graybiel et al. 1977
; Lackner and Graybiel 1984
).
, 1996a
,b
; Cohen 1970
, 1997
; Welch et al. 1996
), and recently the influence of transient Coriolis forces on pointing movements has been studied (DiZio and Lackner 1995
; Lackner and DiZio 1994
). The present study investigates the combined influences of centrifugal and Coriolis forces on reaching.
) in relation to the room, and the angular velocity (
) of the room: FCor =
2m(
×
). The placement of subjects in the room thus affects the magnitude and direction (relative to the body) of Fcent but not FCor, as illustrated in Fig. 1. As a consequence, identical transient Coriolis force perturbations of the arm can be achieved while the body is exposed to different, static G force backgrounds by relocating the subject within the room and keeping
constant.
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FIG. 1.
Illustration of Coriolis (FCor) and centrifugal forces (Fcent) during reaching movements made in the on-center and off-center experimental conditions in the rotating room. Coriolis forces exist on mobile body parts (just the arm in the illustration), they always act orthogonally to movement direction, and their magnitudes are proportional to the rotational velocity of the room ( ), and the arm's mass (m) and linear velocity (
) within the room; Fcor =
2m(
×
). During rotation, centrifugal forces act on both the moving arm and the immobile body parts of the subject, in a fixed direction relative to the room and with a magnitude proportional to the distance from the center (r) and the square of the rotation rate, Fcent =
2r. In this experiment, each subject reached forward parallel to his or her midline 40 times pre-, per, and postrotation. Ten pointed radially outward from the center (cross), and ten sat near the wall and pointed toward the center. When the room was rotating 10 rpm counterclockwise, a rightward Coriolis force was generated in both conditions, ~0.2 g peak. In the on-center condition, the start position for each reach was exactly on the axis of rotation, so the centrifugal force was 0 on the hand and <0.04 g on the rest of the body. In the off-center condition, the subject reached 35 cm toward the center from a start position at a radius of 2.23 m. Centrifugal force on the hand was 0.25 g (resultant equal 1.031 g) at the start position and 0.21 g with the arm extended forward, resisting the direction of movement.
equilibrium point model (Bizzi et al. 1992
), and the
equilibrium point model (Feldman 1986
) predict that movement endpoint accuracy should not be affected by Coriolis force perturbations of movement trajectories because the perturbing force vanishes as the velocity of the arm approaches zero. We found, however, that the reaching movements of subjects seated in the center of a rotating room and pointing to targets are deviated in the direction of the Coriolis forces generated (DiZio and Lackner 1995
; Lackner and DiZio 1994
). The movements ended to the side of the targets in the direction that the Coriolis force acted when the arm was in motion, and the trajectories were more curved than usual. With repeated movements, the subjects rapidly returned to accurate straight line reaches. Full accuracy was regained within ~15 reaches when subjects were denied visual feedback about the position of their hand in relation to the target during their movements; with visual feedback, adaptation to the Coriolis perturbations was more rapid and occurred within ~8-10 reaches. [This adaptation is much more rapid than that which occurs for mechanical perturbations of limb movements (cf. Shadmehr and Mussa-Ivaldi 1994
) to targets. Unlike the case of mechanical perturbations, when adaptation to Coriolis perturbations is complete, the disturbing Coriolis force is no longer perceived as being present even though it is.] After the subjects were brought to rest, their first reaching movements were mirror images to those first made during rotation. In other words, they exhibited a persistence of recalibration and had to readapt to the stationary environment.
), the findings demonstrated that adaptation occurs because the proprioceptive and somatosensory feedback during the movements did not correspond to that which would normally accompany the intended movements. New motor commands became associated with the intended movements that had the consequence of precisely compensating for the Coriolis forces and restoring reaching accuracy.
). In 0 g there is an underdamping of movements with undershoots of intended position, and in 1.8 g the opposite pattern occurs. The magnitude of vibratory myesthetic illusions elicited by tendon vibration is also influenced by background force level (Lackner et al. 1992
), indicating that muscle spindle output or its central processing is modulated by G. We have also found that when the unseen arm is deviated by Coriolis forces in parabolic flight, its felt deviation is larger than normal in 1.8 g and almost abolished in 0 g (Lackner and DiZio 1989
, 1992
). These modulations of proprioceptive function are probably due in part to descending signals stemming from otolith stimulation or propriospinal influences resulting from the altered effective weight of the body.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). After the subject had completed the 40 per-rotation reaches, the SRR was decelerated to rest at 1°/s2. After at least 1 min at 0 rpm, during which no voluntary movements of the head or arms were made, the subject made the postrotation reaches. These movements completed the subject's task.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 2.
Graphs of the average (n = 10, both groups) endpoint and trajectory errors relative to prerotation baseline values during and after exposure to rightward Coriolis forces on the hand in 1-g and 1.031-g force backgrounds. Error bars indicate 1 SE. The initial per-rotation (per, initial) reaching errors represent the deviations elicited when Coriolis forces are 1st introduced. The final per-rotation (per, final) errors gauge the extent of reduction in Coriolis force-induced deviations achieved after 40 reaches. The initial postrotation errors (post, initial) reveal whether automatic motor adjustments acquired during repeated exposure to Coriolis forces are retained when the Coriolis forces are 1st absent.
0.2 g, peak) that developed as the peak movement velocity was approached. As the reaching movements slowed and the Coriolis forces diminished, the hand tended to return toward the target but stopped considerably off to the right side. The average lateral endpoint error (difference from baseline) was 40 mm for the on-center group and 37 mm for the off-center group, the average error in curvature was 23 mm rightward for the 1-g group and 18 mm rightward for the off-center group. These lateral endpoint and trajectory errors were significantly larger than zero [correlated t-tests; t(9) > 3.140, P < 0.012] for both groups, but were not significantly different between the groups. The movement trajectories are illustrated in Fig. 3. The distance of per-rotation reaches was slightly but not significantly shortened relative to baseline for both groups, and the extent of this shortening was not different between groups.
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FIG. 3.
Top views of the initial and final (40th) pre-, per-, and postrotation reaching movements sampled at 100 Hz and averaged for the 10 subjects in the 1-g and 1.031-g test conditions. Prerotation movements are straight and accurate. In both 1 g and 1.031 g, initial per-rotation movements are deviated to the right and end to the right, the direction of the Coriolis force generated. In 1 g, the final per-rotation movements are identical to prerotation, but in 1.031 g the endpoints remain deviated rightward although the path becomes straight again. Postrotation movement patterns mirror the initial per-rotation ones with the important difference that the initial endpoint errors are smaller in 1.031 g than 1 g. There are no changes in reaching distance.
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FIG. 4.
Plots of lateral endpoint and trajectory curvature for all 120 reaches of an experimental session, averaged across subjects for the 1 g (top plots) and 1.031 g (bottom plots) test groups. Endpoints are deviated right of baseline by the introduction of Coriolis forces and return all the way to baseline within ~15 per-rotation reaches for the 1-g force group. Improvement stops after the 1st 8 per-rotation reaches without full return to baseline for the 1.031-g group. By contrast, trajectory curvature shows return to baseline values for both groups.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
(Bizzi 1980
; Bizzi et al. 1976
, 1992
) and
models (Feldman 1966a
,b
, 1974
, 1986
). These theories are of direct relevance to motor control in artificial gravity environments because they have to predict that the trajectories of movements should be deviated by the transient Coriolis forces but that the endpoints should not. From the equilibrium point perspective, movement is controlled by an evolving set of motor commands that specify changing length-tension relations of the relevant muscles. Transient perturbations (e.g., such as the Coriolis forces in our experiment) are predicted to deflect the trajectory only temporarily because the programmed endpoint of the movement is achieved by agonist-antagonist activation patterns that create a static equilibrium position determined by the controlled, elastic properties of the muscles. The highly significant endpoint errors initially exhibited by all of our subjects exposed to Coriolis forces (forces that vanish at the end of the movement) indicate that equilibrium point theories are incorrect in their basic prediction. In fact, errors are initially present, and one does have to adapt limb movement control in an artificial gravity environment to attain prescribed target configurations of the limb.
, 1994
; Lackner and Graybiel 1981
, 1982
). Such reprogramming is automatic and persists when rotation stops, which is why the initial per-rotation and initial postrotation reaches are mirror images of each other (see Fig. 4).
). These results, along with other observations we have made studying tonic vibration reflexes in parabolic flight (Lackner et al. 1992
), strongly suggest that alterations in muscle spindle activity occur as a function of background force level. Spindle sensitivity seems diminished in 0 g and enhanced in 1.8 g; such changes can be understood on the basis of otolith-spinal modulation of spindle gain (cf. Watt et al. 1986
). They are also consistent with recent observations on pointing movements during prolonged exposure to microgravity (Watt 1997
). Golgi tendon organ activity must also be altered in different gravitoinertial force backgrounds because of the alteration in effective body weight and different muscle forces necessary to maintain postural configuration.
).
, 1996
) including one involving vestibular loss patients (DiZio and Lackner 1996
). The labyrinthine-defective subjects showed normal trajectory adaptation but incomplete endpoint adaptation. Interestingly, the muscle spindle primary and secondary systems are normally modulated by vestibular signals. Spindle primaries contribute signals related to muscle velocity and length and spindle secondaries to muscle length. In terms of adaptation of movement control, it is likely that the spindle primaries are involved in adaptation of movement endpoint (the length signal) and shape (the velocity signal) and spindle secondaries in movement endpoint (the length signal). With alteration of spindle gain owing to labyrinthectomy or to changed background force level, the dynamic response seems to be better preserved than the static allowing trajectory path adaptation but diminished movement endpoint adaptation. Our evidence of independent adaptation of movement trajectory curvature and endpoint shows that CNS mechanisms monitor and represent them distinctly, although in actual execution they are normally implemented synergistically.
, 1998), we have shown that subjects experiencing illusory, rotary self-displacement show reaching errors to targets. These errors reflect automatic compensations that are being made for the Coriolis forces that would be present during the reaches if the subjects were actually rotating. These observations indicate that virtual reality systems inducing apparent self-displacement will affect sensory-motor control. We are currently exploring how adaption acquired to virtual rotation transfers to real rotation and vice versa. These are issues of fundamental importance both for theories of motor control as well as the possible use of artificial gravity in long-duration space missions.
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ACKNOWLEDGEMENTS |
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We thank Y. Altshuler, E. Kaplan, A. Kanter, and J. Ventura for technical assistance.
This work was supported by National Aeronautics and Space Administration Grants NAGW-4733, NAGW-4374, and NAGW-4375.
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FOOTNOTES |
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1 An analysis of artificial gravity can also be made without reference to centrifugal forces that are inferred inertial reaction forces in a rotating framework. The alternative approach is in terms of centripetal forces contributed by the "floor" of the rotating vehicle providing forces directed toward the spin axis. Centripetal forces are analogous to terrestrial ground reaction forces on objects that oppose the gravitational pull.
2 G refers to the gravitoinertial resultant vector. This is the vector sum of the gravitational force, g, and the inertial forces present. It is conveniently expressed in multiples of g units with g being 9.8 m/s2.
Address reprint requests to J. R. Lackner.
Received 9 February 1998; accepted in final form 17 April 1998.
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REFERENCES |
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