Ashton Graybiel Spatial Orientation Laboratory and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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ABSTRACT |
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DiZio, Paul and James R. Lackner. Congenitally Blind Individuals Rapidly Adapt to Coriolis Force Perturbations of Their Reaching Movements. J. Neurophysiol. 84: 2175-2180, 2000. Reaching movements made to visual targets in a rotating room are initially deviated in path and endpoint in the direction of transient Coriolis forces generated by the motion of the arm relative to the rotating environment. With additional reaches, movements become progressively straighter and more accurate. Such adaptation can occur even in the absence of visual feedback about movement progression or terminus. Here we examined whether congenitally blind and sighted subjects without visual feedback would demonstrate adaptation to Coriolis forces when they pointed to a haptically specified target location. Subjects were tested pre-, per-, and postrotation at 10 rpm counterclockwise. Reaching to straight ahead targets prerotation, both groups exhibited slightly curved paths. Per-rotation, both groups showed large initial deviations of movement path and curvature but within 12 reaches on average had returned to prerotation curvature levels and endpoints. Postrotation, both groups showed mirror image patterns of curvature and endpoint to the per-rotation pattern. The groups did not differ significantly on any of the performance measures. These results provide compelling evidence that motor adaptation to Coriolis perturbations can be achieved on the basis of proprioceptive, somatosensory, and motor information in the complete absence of visual experience.
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INTRODUCTION |
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Reaching movements to visual
targets are generally relatively straight (Morasso
1981). However, the paths of reaches made to visual targets
during constant velocity rotation in a fully enclosed slow rotation
room (SRR) are curved, and the endpoints are displaced relative to the
targets in the direction opposite rotation. The curvature and endpoint
errors are the result of inertial Coriolis forces generated by the
movement of the arm relative to the rotating environment
(Lackner and DiZio 1988
, 1994
). Figure
1 illustrates the experimental situation.
If additional reaches to visual targets are made during rotation, the
movement paths become straighter and the endpoints more accurate. This improved performance occurs even if subjects are denied visual feedback
about the paths of their movements, although adaptation occurs with
about half as many movements if continuous visual feedback is
permitted.
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Several studies have identified the importance of vision in affecting
both the path and accuracy of goal-directed arm movements. Desmurget et al. (1997) have demonstrated that sight of
the pointing hand prior to movement initiation enhances the accuracy of
target attainment with that hand. Miall and Haggard
(1995)
and Sergio and Scott (1998)
have shown
that the reaching movements of blind subjects and of blindfolded,
sighted subjects to haptically specified targets are more curved than
movements made by the sighted subjects to the same target positions
under visual guidance. Wolpert et al. (1994)
and
Flanagan and Rao (1995)
have provided evidence underscoring, respectively, how visual misperception of curvature can
affect the path of movements and how visual feedback about hand or
joint space influences whether hand or joint trajectory is linearized.
Yet other studies have highlighted vision as being the "distal
teacher" used to update internal models of self and environment (e.g., Jordan 1995; Jordan and Rummelhart
1992
; Kawato and Gomi 1992
; Miall and
Wolpert 1996
; Wolpert 1997
; Wolpert and
Kawato 1998
). Vision also figures prominently as the feedback
source for updating motor control when a mechanical manipulandum that controls the position of a visual cursor is sytematically perturbed as
subjects attempt to bring the cursor in register with visual targets
(Shadmehr et al. 1993
). Desmurget et al.
(1999)
using trans-cranial magnetic stimulation have
very recently found evidence that the posterior parietal cortex (PPC)
figures importantly in the planning and updating of reaching movements
to visual targets. In their view, PPC computes both a forward model of
instantaneous hand location and a dynamic motor error signal indicating
the difference between ongoing hand position and visual target location.
These various studies raise the possibility that subjects in the SRR
experiments who point to the locations of just extinguished visual
targets may show adaptive changes in reaching behavior that are
contingent on visual experience. The visual target present before
movement onset is clearly involved in the motor planning of the
reaching movement, and a dynamic error signal may be maintained of the
position of the hand relative to the target position even though the
visual target is extinguished with the onset of the movement. This
would be consistent with the role of PPC proposed by Desmurget
et al. (1999), and with a large body of evidence implicating
vision in the calibration of proprioception and in the adaptive process
(Ghilardi et al. 1995
; Helms-Tillery et al. 1991
; Sainburg et al. 1993
, 1995
;
Vindras et al. 1998
). It also would be consistent with a
large body of evidence implicating visual and motor imagery in
performance enhancement (Crammond 1997
). It is also
conceivable that the presence of a visual target affects the accuracy
of arm position registration. Ghez and Sainburg (1995)
have shown that improvements in movement performance attained through
visual feedback transfer to nonpracticed directions when subsequent
movements are made visually open-loop. The performance enhancement is
present for normal subjects and patients without limb proprioception.
Ghez and Sainburg make the important proposal that subjects are
acquiring a general rule that becomes part of an internal model of limb
dynamics rather than a specific movement pattern.
To determine whether subjects can adapt to Coriolis force perturbations of their reaching movements in the absence of vision, we tested two groups of subjects. One group consisted of congenitally blind subjects who had never experienced light sensations. The other group included normal sighted subjects who were in total darkness during testing. Our approach was to have the blind and control subjects reach to a haptically specified goal position on a surface in front of them before, during, and after exposure to constant velocity rotation in the SRR.
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METHODS |
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Subjects
Five congenitally blind subjects who had never experienced light sensations participated after giving informed consent to the experimental protocol. They ranged in age from 19 to 44 yr old (see Table 1). In addition, five normally sighted individuals of comparable ages participated as a control group. All were healthy and physically active, and all were right-handed. They were tested in total darkness. None of the subjects was familiar with the goals of the experiment nor had had previous experience in rotating environments.
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Apparatus
The experiment was conducted in the Graybiel Laboratory SRR, a fully enclosed chamber 6.7 m diam. The subject was seated in a chair located over the center of rotation so that the start position of his or her right hand corresponded to the center of rotation. This positioning ensured that there were no significant unusual forces acting on the subject's arm or on his vestibular system at the beginning or end of a reaching movement. A contoured headrest was used to stabilize the subject's head. A smooth horizontal Plexiglas surface extended in front of the subject at waist level. A subject's reaching movements started and ended with contact with this surface. A WATSMART motion analysis system was used to record the path and endpoint of each movement by tracking an infrared emitter taped to the tip of the index finger of the pointing, right hand. Sampling rate was 100 Hz. Figure 1 illustrates the test situation.
Procedure
Each test session included pre-, per-, and postrotation reaches, always with the right hand. The sighted, control subjects were brought into the test chamber with their eyes closed and were kept in total darkness throughout the experiment. The subjects started each reach from a microswitch on the Plexiglas surface near their midline. The experimenter gave the subject a "target" to point to by moving the subject's hand to a position on the surface 35 cm forward of the "start button" in the midline. This position was demonstrated several times until the subject felt comfortable in localizing the desired target position. The surface was smooth so that there were no distinctive texture cues about the desired target position available from finger contact. Each subject made 40 prerotation, 40 per-rotation, and 40 postrotation reaches. The subjects were instructed to reach at a natural, comfortable rate lifting their finger and reaching forward to touch down on the surface at the target location in one continuous smooth movement. They were told to correct their reaching movement if they felt they were making an error but not to stop their movement to do so. On completion of each reach they held their finger in place for about 1 s, raised it, and slowly brought it back to the start button.
When the 40 prerotation movements were completed, the SRR was accelerated to a constant velocity of 60°/s counterclockwise (CCW) at 1°/s2. After 2 min at constant velocity, the per-rotation movements were made. Following completion of the per-rotation reaches, the room was decelerated to rest at 1°/s2. After a 2-min interval, the postrotation movements were made. Throughout the experiment, when the subjects were not making movements to the "target," they avoided making any head or arm movements. The subjects were asked after each set of eight reaching movements whether they felt any sense of rotation. All of the subjects indicated that they always felt completely stationary during the testing periods.
Data analysis
A computer algorithm determined the end position and duration of each reaching movement. The end corresponded to the location where movement velocity fell below 3% of peak velocity. The maximum deviation of the movement path from a straight line connecting the movement start and end position was calculated and used as an index of path curvature. Each subject's final eight prerotation reaches were averaged to serve as a baseline for comparison with per- and postrotation reaches.
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RESULTS |
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The experimental results are summarized in Table 2 and presented graphically in Figs. 2 and 3. As can be seen, the pattern is one of per-rotary deviation of trajectory and endpoint with complete adaptation within about 10 reaches; mirror image aftereffects on cessation of rotation, and complete decay of aftereffects within 10 reaches. To quantify the rate of adaptation and readaptation, we computed for each subject the number of movements required for the endpoint curvature deviations to diminish to 10% of their magnitudes in the initial per- and postrotation reaches. The averages across subjects for both groups are presented in Table 3. We first describe below the patterns characteristic of the blindfolded control and the blind subject groups and then present a statistical analysis of the data.
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Prerotation reaches
The normal control subjects and blind subjects reached in slightly
curved paths (viewed from above). The average peak path deviation of
the baseline reaches from a straight line was 16 mm (left of midline)
for the control subjects and
19 mm for the five congenitally blind
subjects. Movement endpoints were 43 mm right of the midsagittal plane
for the blind subjects and 4 mm to the left for control subjects.
Per-rotation reaches
The initial per-rotation reaches of the normal control subjects deviated rightward paralleling the development of the rightward acting Coriolis forces and then inflected leftward as the Coriolis forces abated. The average peak curvature was +17 mm, a change of 33 mm rightward. The average endpoint of these reaches, relative to prerotation baseline, was deviated 44 mm rightward, in the direction of the prior acting Coriolis force. With additional reaches, movement paths became straighter and endpoints more accurate, until after about 12 reaches the movement trajectories and endpoints were back to prerotation baseline values.
The blind subjects' initial per-rotation reaches were also deviated in the direction of the transient Coriolis forces. The average peak curvature was +8 mm, a 27-mm rightward shift relative to baseline. The average movement endpoint was also displaced in the direction of the Coriolis force, 35 mm rightward of baseline value. With additional reaches, movement paths became more and more like those of the prerotation baseline reaches, and the endpoints of the movements also returned toward baseline values. After about eight or nine per-rotation reaches, movement trajectory curvatures and endpoints, respectively, were back to their prerotation baseline values.
Postrotation reaches
The initial postrotation reaches of the control subjects had
movement paths mirror symmetric to the initial per-rotation reaches. The movements deviated leftward and then returned somewhat toward the
midline but still ended significantly displaced leftward relative to
the prerotation endpoint baseline. The average peak curvature was 33
or 17 mm more leftward than baseline; the average endpoint was 14 mm
left of prerotation baseline. As additional reaches were made, the
movements gradually became straighter and more accurate, until after
about seven reaches they were indistinguishable from baseline values.
The blind subjects' initial postrotation reaches also showed mirror
symmetric changes in movement path, curving leftward in relation to
initial per-rotation paths, returning rightward toward the end of the
movement, and ending to the left of the target goal position. Average
peak curvature was
41 mm and average endpoint 11 mm left of baseline.
After six additional reaches, movements returned to their
characteristic prerotation baseline curvature, and after 10 regained baseline endpoint accuracy.
In the prerotation period, the blind subjects had significantly
different baseline endpoints (P = 0.021 in a
t-test) from the controls, but the curvature of their
movements was statistically indistinguishable. Our analysis focused on
deviations from the prerotation baselines, which reflect the amplitudes
of Coriolis force perturbations and adaptive compensations. An initial
ANOVA showed that there was no difference between the subject groups in
deviations from baseline of trajectory curvature, endpoint accuracy, or
variability. Separate ANOVAs performed for each group showed
significant (P < 0.001) endpoint and curvature
differences across the baseline, initial and final per-rotation, and
postrotation movements. The means of pairs of conditions were compared
with Tukey post hoc tests with < 0.05 as the criterion for
significant differences. Both groups showed significant differences
between their prerotation baselines and their initial per-rotation
reaches for both trajectory curvature and endpoint reflecting the
influence of the transient Coriolis force perturbations. The initial
and final per-rotation reaches within each group were also
significantly different for curvature and endpoint indicating the
acquisition of adaptation. The curvatures and endpoints of the final
per-rotation reaches were not different from prerotation baseline
indicating complete adaptation. The initial postrotation reaches
differed for each group from prerotation baselines, both for endpoint
and curvature, reflecting the persistence of the adaptive compensations acquired during rotation. The final prerotation and final postrotation reaches were not different in either curvature or endpoint within the
groups, indicating complete readaptation to the stationary environment.
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DISCUSSION |
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In their prerotation baseline reaches, both subject groups pointed
to the haptically specified target location in curvilinear paths,
unlike subjects in our earlier experiments who had pointed to the
location of just extinguished visual targets in essentially straight
paths (cf. Lackner and DiZio 1994). The extent and
direction of curvature exhibited by our subjects are directly
comparable to that reported by Miall and Haggard (1995)
and Sergio and Scott (1998)
for their blind subjects and
blindfolded, sighted subjects making comparable forward directed
movements. Moreover, our blind and control subjects, like theirs, did
not show significant intergroup differences in curvature for this
movement direction.
Our control subjects and our congenitally blind subjects exhibited
comparable deviations of movement path and endpoint during their
initial per-rotation reaches when they were first exposed to Coriolis
forces. None of them had had prior experience making arm movements
during passive constant velocity rotation, so they were not expecting
their arm movements to elicit unusual forces. Many expressed surprise
after their first movements and said their arm had not done what they
had intended. With additional movements, both groups' reaching
movements became more and more similar in curvature and endpoint to
their prerotation reaches. After about 10 additional per-rotation
movements, each group was back at prerotation baseline values.
Consequently, these findings demonstrate that adaptation to Coriolis
force perturbations does not require visual specification of target
position, visual feedback about movement path or endpoint, nor visual
imagery about movement performance. Our congenitally blind subjects,
for example, have never experienced visual sensations. Thus vision is
sufficient but not necessary as a distal teacher for updating motor
control. In ongoing studies, we have found that subjects allowed
continuous sight of their arms during exposure to Coriolis forces
achieve full adaptation with about 40% fewer movements than those
tested in total darkness. This improvement is present at all rotational
velocities tested, 5, 10, 15, and 20 rpm (Siino-Sears et al.
2000). It is consistent with and supportive of Ghez and
Sainburg's proposal, discussed in the INTRODUCTION, that
vision can update the internal model of limb dynamics in a general
nonmovement specific fashion.
The updating of internal models of inverse dynamics and expected
regularities of the environment is manifest in our subjects' initial
postrotation reaches. These reaches have mirror image symmetry to their
initial per-rotation reaches that were deviated by Coriolis forces. The
nature of these aftereffects indicates that the nervous system has
computed the Coriolis force "expected" for the movement being
executed and has programmed a compensation appropriate to cancel the
consequence of this force. Postrotation, this compensation is no longer
appropriate, hence the pattern of aftereffects. However, both during
constant velocity and postrotation, the subjects feel stationary.
Consequently, they register the context as being the same [the issue
of context specificity is further discussed in Cohn et al.
(2000)]. Interestingly, during rotation after the subjects
have adapted, they no longer feel the Coriolis forces generated by
their movements. These forces become perceptually transparent, and
their movements seem totally normal. By contrast, postrotation when
subjects first make reaching movements, they report feeling a force
deviating their arm. All subjects in all of our experiments on
adaptation to Coriolis forces report this (cf. DiZio and Lackner
1995
; Lackner and DiZio 1994
). They are
experiencing their CNS's compensation for expected but absent Coriolis
forces as an external force.
Current models of movement control tend to place great emphasis on
vision for updating movement control parameters. Our findings emphasize
the importance of a cooperative interaction and interrelating of
somatosensory, proprioceptive, and efferent signals, along with visual
ones, in updating control. In fact, we know from other contexts that
somatosensation and proprioception can be as important as vision in
guiding motor control. For example, individuals without labyrinthine
function cannot stand heel to toe for more than a few seconds without
losing balance even when permitted sight of their surroundings.
Nevertheless, they can stand in this posture indefinitely with eyes
closed if they are permitted to touch a stable surface very lightly
with their index fingertip (Lackner et al. 1999). The
finger contact, although below force levels adequate to provide any
mechanical stabilization, provides spatial cues about the direction of
body sway. By minimizing the tiny force changes at the fingertip, body
posture is "automatically" stabilized.
In the present experimental situation, subjects had to rely on
somatosensory and proprioceptive feedback for initially specifying the
target position and later for controlling and adjusting their movements
to achieve the target position. We have demonstrated recently that when
the hand makes contact with a surface at the end of a reaching
movement, the magnitude and direction of contact shear forces on the
fingertip provide a spatial directional map of finger position relative
to the body (DiZio et al. 1999). Each location on a
surface is associated with a different pattern. These terminal landing
cues allow endpoint adaptation to occur, but provide no information for
adaptation of movement path, which has been shown to be dissociable
from movement endpoint adaptation (DiZio and Lackner
1995
). The unusual pattern of muscle spindle feedback
associated with Coriolis perturbed movements provides information about
unexpected movement curvature allowing adaptive modifications to be
introduced (Lackner and DiZio 1994
,
2000
). The increase in spindle activity in the
muscles stretched by the Coriolis-induced displacement of the arm over
that appropriate for the movement intended signals the direction of
deviation of the arm. The temporal pattern of this activity provides
information about the curvature of the movement. These patterns allow
the CNS to model the Coriolis force and gradually compensate for its presence in future movements. Thus fingertip cutaneous receptors and
brachial mechanoreceptors are sufficient to specify target location,
provide feedback about arm location and path, and possibly contribute
to a spatial image of hand position.
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ACKNOWLEDGMENTS |
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We thank E. Kaplan, V. Siino-Sears, and J. Ventura for technical assistance. We thank an anonymous reviewer for mentioning the possible importance of nonvisual spatial imagery.
This research was supported by National Aeronautics and Space Administration Grants NAG9-1037 and NAG9-1038.
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FOOTNOTES |
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Address for reprint requests: P. DiZio or J. R. Lackner, Graybiel Lab, MS 033, Brandeis University, 415 South St., Waltham, MA 02454 (E-mail: dizio{at}brandeis.edu or lackner{at}brandeis.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 19 April 2000; accepted in final form 6 June 2000.
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REFERENCES |
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