1Research Service (151S), Veterans Affairs Medical Center, Syracuse, New York 13210; and 2Institut des Sciences Cognitives, 69675 Bron, France
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ABSTRACT |
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Clower, Dottie M. and Driss Boussaoud. Selective Use of Perceptual Recalibration Versus Visuomotor Skill Acquisition. J. Neurophysiol. 84: 2703-2708, 2000. Exposure to laterally displacing prisms is characterized by systematic misreaching in the opposite direction after prisms are removed. Other learning tasks involving altered visuomotor mappings can often be mastered by the subject with minimal resulting aftereffects. One variable that may account for this difference is the nature of the feedback provided to the subject: during studies of prism exposure, subjects usually view the hand itself, whereas in many studies of visuomotor learning, subjects view a computer-generated representation of the hand position or movement. We compared the use of actual feedback of the hand with computer-generated representational feedback of its position during exposure to laterally displacing prisms. In the actual feedback condition (ACT), a light on the fingertip was illuminated immediately at the end of each reach. In the representational feedback condition (REP), a computer-generated spot of light was displayed to indicate the exact position of the fingertip at the end of each reach. Whereas the rate and magnitude of error correction were the same in both conditions, only the ACT condition produced the large adaptive aftereffect typically observed after prism exposure. These results suggest that the perception of a physical coincidence between the feedback source and the hand may be a key factor in determining whether adaptation is accomplished through perceptual recalibration or visuomotor skill acquisition.
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INTRODUCTION |
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The advent of modern technology has brought with it a new repertoire of motor skills that require a relatively novel form of eye-hand coordination. When we point to objects on our computer monitor by controlling a cursor with a "mouse," the correspondence between the movement of the hand and its effect on the visual object is not direct; what we observe on the screen represents our hand movement. Under such representational conditions, we must practice to establish the correct relationship between visual input and motor output, or in other words, we must adapt to the new visuomotor arrangement. Once acquired, competent performance of the visuomotor relationship may persist for years and does not interfere with our ability to learn or perform other visuomotor tasks. Such are the characteristics typically attributed to visuomotor skill acquisition, or acquisition of a kinematic "internal model."
Laterally displacing prisms also produce a visuomotor rearrangement
that leads to adaptation during exposure. Yet fundamental differences
exist in the profile of psychophysical responses observed after prism
adaptation when compared with acquisition of a novel visuomotor
arrangement in a representational workspace environment. For example,
studies examining states of dual adaptation to prisms have had
difficulty demonstrating robust multi-state retention comparable to
that observed with multiple "internal models" (Flook and
McGonigle 1977; Kurata and Hoshi 1999
;
Welch et al. 1993
). Such disparate psychophysical
manifestations have led others to emphasize the distinction between
visuomotor skill acquisition (i.e., a task-dependent
adjustment of the motor response to compensate for a manipulation of
the working environment) and perceptual recalibration (i.e.,
a coordinative remapping between different perceptual representations
such as vision and proprioception) (Bedford 1993
;
Lackner and DiZio 1994
; Martin et al.
1996b
; Redding and Wallace 1996
).
Perceptual recalibration appears to involve a global topological
realignment, in that alterations within a trained region of space
generalize to other untrained regions (Bedford 1993). Recalibration also shows limited intermanual transfer and produces directional aftereffects that indicate a difficulty in returning to the
original visuomotor mapping even with cognitive awareness of the change
(Bedford 1993
; Harris 1965
;
Uhlarik 1973
). Robust aftereffects are commonly observed
in studies of adaptation to prisms and are consistent with the view
that the adaptive response to prismatic displacement of the visual
field is primarily due to perceptual recalibration (Held and
Hein 1958
; Mather and Lackner 1981
; Welch
1986
).
Visuomotor skill acquisition, on the other hand, is characterized by an
ability to establish a nontopological relationship between visual input
and motor output (i.e., generalization to untrained regions is less
likely), the capacity to maintain multiple noncompeting visuomotor
mappings, and substantive intermanual transfer (Cunningham and
Welch 1994; Ghahramani and Wolpert 1997
; Imamizu and Shimojo 1995
). In addition, directional
aftereffects from exposure are rarely observed, and when noted are
substantially less than those found with adaptation to prisms. For
example, after learning a new visuomotor mapping in which the direction of cursor movement is rotated compared with the hand movement, monkeys
and humans were able to revert to normal performance on the standard
mapping condition with only minimal directional
aftereffects1
(Cunningham and Welch 1994
; Flanagan and Rao
1995
; Tamada et al. 1999
; Wise et
al. 1998
). As in the current paper, others have cited the
relative absence of aftereffects as an indicator of a skill acquisition
process as opposed to a recalibrative process (Lackner and DiZio
1994
; Martin et al. 1996b
; Redding and
Wallace 1996
).
While different psychophysical manifestations of perceptual
recalibration and visuomotor skill acquisition have been observed, it
is unclear what factors might lead to the selective employment of one
type of adaptation or the other. One hypothesis is that the perceived
source of the error may play a key role in determining which mechanism
is likely to be employed. Under some experimental circumstances, such
as when the displaced limb is viewed directly through prisms, the
discrepancy between visual and proprioceptive feedback may be
interpreted as a misalignment of internal representations of the two
modalities. Such a perceived "internal error" may engage mechanisms
to reestablish the proper registration, resulting in a perceptual
recalibration or realignment, and a resultant aftereffect in
postexposure testing (Bedford 1999). However, if
feedback were provided that was not necessarily perceived as physically
coincident with the limb, as may be the case when using
computer-generated feedback, then the discrepancy could be considered
to arise from manipulation of the working environment. Under such
conditions, the perceived "external error" might facilitate an
indirect mapping strategy that would allow for a context-specific
adjustment of the motor response without an accompanying perceptual recalibration.
Studies of prism adaptation have typically utilized vision of the hand itself, or a light source attached to the hand, to provide the necessary feedback to the subject. In comparison, other studies of visuomotor learning have typically used computer-generated feedback that is not physically coincident with the hand itself. In the current experiment, we test the hypothesis that the perceived physical coincidence of the feedback in prism adaptation may be a critical factor in assigning the source of the visuomotor discrepancy. We measured subjects' reaching accuracy before, during, and after exposure to laterally displacing prisms under two conditions: one in which they received actual feedback of their hand position immediately after each reach via a light-emitting diode (LED) attached to the index finger, and another in which they received (identically positioned and timed) representational feedback of the reaching endpoint via a computer-generated spot of light.
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METHODS |
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Subjects
Experiments were performed in accordance with applicable guidelines for the use of human subjects. Four males and two females, mean age 32 yr, gave informed consent to participate in the study. All subjects had normal or corrected to normal vision, and all were right-handed except one female, who performed the task with her right hand. Before the experiment began, subjects were informed of the effects of prisms, and that the current study was designed to examine the effect of different types of feedback on reaching accuracy after prism exposure. They were instructed that the light presented during the feedback phase would indicate the position of their finger, and that they should try to reach to the targets as accurately as possible.
Apparatus
The subject was seated in front of a resistive touchscreen (36 × 27 cm) inclined at a 45° angle. A semi-reflective mirror was positioned above the touchscreen, such that targets projected onto the mirror (from a computer monitor suspended above the head of the subject) appeared to the subject to be located on the touchscreen. Reaching movements originated from a homepad located at the subject's midline in front of (but not in contact with) the chest, and terminated on the touchscreen surface beneath the level of the semi-reflective mirror, with a reaching distance of approximately 30 cm (Fig. 1). The subject's head was restrained with a padded chin rest and straps around the forehead. A practice period consisting of 10 reaches performed under ambient lighting conditions was completed before the experiment began. Experiments were performed in total darkness and typically lasted for a period of 20-30 min.
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Procedures
The design of the two conditions followed the standard pattern of testing employed in most studies of prism adaptation. An assessment of each subject's reaching accuracy to visual targets was performed (preexposure), followed by a period during which the subject reached to targets and obtained feedback of accuracy while wearing prisms (exposure), followed by a repeat assessment of reaching accuracy once the prisms were removed (postexposure). In each of these phases, the subject made 10 reaches to each of 5 potential targets organized along the horizontal plane for a total of 50 reaches per phase. Each individual trial was initiated when the subject placed his or her hand on the homepad.
PREEXPOSURE. A circular red target (2° diameter) was displayed for 1 s and then extinguished. After a 2-s delay, a beep instructed the subject to reach from the homepad to the remembered location of the target. The subject received no information about reaching accuracy. After the subject returned his hand to the homepad, the next target was displayed.
EXPOSURE. A 10-diopter wedge prism that created a 5.8° leftward displacement of the visual field was placed in front of the subject's right eye (a patch over the left eye remained in place throughout the entire experiment). Because the prisms would cause the targets to appear farther to the left than in the other conditions, the target positions were adjusted 5° to the right by the paradigm control software to compensate for the visual displacement. This way, the targets appeared to the subject to be located in approximately the same place during each phase of the experiment. Precisely when the subject's finger contacted the touchscreen, the target and the feedback source were illuminated for 200 ms. During this time, the subject's hand remained stationary on the touchscreen. After the feedback period, the subject returned his or her hand to the homepad to initiate the next trial.
POSTEXPOSURE. The wedge prism was removed, and the targets were readjusted to their original position by the computer software. The subject reached to targets as they had in the preexposure phase, with no feedback about reaching accuracy.
Each subject performed the task under two conditions during different sessions (separated by at least 3 days) and in a randomized order. The two conditions were identical with respect to the magnitude of prismatic displacement, pre- and postexposure testing phases, and timing and duration of feedback; only the nature of the feedback signal was varied.ACTUAL FEEDBACK CONDITION (ACT). A small LED (0.3° diam) was taped to the subject's right index finger at the beginning of the experiment. The placement and intensity of the LED were adjusted to minimize any potential illumination of the fingertip. During the exposure phase, the target and the LED on the finger were illuminated for 200 ms at the end of each reaching movement, while the hand remained stationary. Due to the semi-reflective nature of the mirror, the subject was able to see the LED position in relationship to the target such that for accurate reaches, the two were superimposed. When reaches were inaccurate, the subject could compare the two positions to evaluate the magnitude and direction of the error.
REPRESENTATIONAL FEEDBACK CONDITION (REP). At the termination of each reach, the computer software reproduced the position of the subject's touch by displaying a small white square (0.3°). The target was also illuminated, so that its position could be compared with the reach endpoint during the 200-ms feedback interval. The position of the square precisely reflected the position of the unseen fingertip below, such that there was no discrepancy between finger position and the feedback light other than that produced by the prismatic displacement (a situation directly comparable to the ACT condition described above).
Data analysis
Movement time, reaction time, and X/Y coordinates of the target and touch position were recorded for each trial. The horizontal component of the error between the target position and the touch position was calculated in degrees of visual angle for each reach. To establish a subject's baseline reaching accuracy, the errors for all preexposure reaches were averaged, providing a "normalization value" for each individual. This normalization value was then subtracted from each error measurement in both the pre- and postexposure phases, such that the adjusted differences could be compared across subjects. In essence, this adjustment normalized each subject's preexposure values to zero and aligned their postexposure values to the preexposure baseline. The significance of each individual's pre- to postexposure shift, as well as the shift for the group, was assessed by Student's two-tailed t-test.
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RESULTS |
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Every subject in the ACT condition had a significant (P < 0.05) aftereffect in the direction indicating an adaptive compensation for the prismatic displacement, while only two of six individuals demonstrated a significant shift in the REP condition (1 of which was in the nonadaptive leftward direction). For the ACT condition, the group displayed an average adaptive aftereffect of 3.40° [t(5) = 4.234, P = 0.008], while in the REP condition, the group had a nonsignificant [t(5) = 1.024, P = 0.353] shift of 0.52°. Figure 2 shows the pre- versus postexposure difference in reaching accuracy for the grouped data.
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The time course of responses during the three phases of each experiment is shown in Fig. 3A. During the preexposure phase, the reaching responses for both the ACT and REP conditions center on zero (which represents each subject's baseline reaching accuracy). As can be seen in the first plotted point of the exposure phase, subjects initially misreached to the left of the target in the presence of the prismatic displacement. Within the 1st 10 trials, subjects modified their reaches to compensate for the prismatic shift in both conditions. In the postexposure phase, the results of the ACT condition displayed the adaptive aftereffect typically associated with adaptation to prisms, while the REP condition showed only a minimal (nonsignificant) effect of the prism exposure.
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A factor that may have contributed to the difference between the two
conditions was the rate at which the subjects corrected their errors
during the exposure phase. Since subjects in both groups regained their
reaching accuracy relatively quickly, we examined the time course of
correction during the initial 10 reaches of the exposure phase. As
shown in Fig. 3B, the profiles for the ACT and REP
conditions were remarkably similar. Both groups demonstrated an initial
error of approximately 5° on the first reach, followed by a gradual
decrease in error over the initial five reaches. After this point, the
reduction of error reached a plateau for both the ACT and REP conditions.
The difference observed between the REP and ACT conditions could also have been caused by the kinematics of the subjects' error-corrective responses to the exposure condition. To assess this possibility, we compared the mean reaching error, the reaction time, and the movement time for the two conditions during the exposure phase. None of these measures demonstrated a significant difference between the two experimental conditions. Mean values for these data (±SD) are shown in Table 1.
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During the 50 postexposure reaches, both conditions demonstrated a
slight improvement in reaching accuracy over time (see Fig.
3A). This decay of the aftereffect is independent of
feedback as the subject received no information about reaching accuracy during this period. It is interesting to note that the slope of this
decay is similar in the two conditions, and is consistent with previous
findings on the rate of aftereffect decay without feedback (Choe
and Welch 1974). To assess whether this decrease in reaching
error may have masked a small but initially significant shift in the
REP condition, a statistical comparison of the 1st 10 reaches (pre- vs.
postexposure) for each condition was performed (comparable to that
shown in Fig. 2). This analysis revealed a significant
[t(5) = 3.863, P = 0.012] aftereffect
of 3.98° for the ACT condition, and a nonsignificant
[t(5) = 1.765, P = 0.138] shift of
1.19° for the REP condition. The average value of the first
postexposure reach in the REP condition was 1.41° (compared with
4.10° in the ACT condition), indicating that even from the very first
reach after exposure, subjects in the REP condition did not demonstrate
an aftereffect comparable to that seen in the ACT condition.
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DISCUSSION |
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In the ACT condition, subjects demonstrated a large aftereffect
like those typically observed after exposure to laterally displacing
prisms. In the REP condition, however, subjects apparently corrected
for the perceived error, but were able to revert to the original
visuomotor mapping once the prisms were removeda pattern most
consistent with visuomotor skill acquisition. The qualitative
difference between the two conditions was the subjects' perception of
physical coincidence with the feedback source.
Differences in cognitive state between the two conditions were unable to account for this result, since all subjects received the same instructions before completing both the REP and ACT conditions. While they were informed about the displacement caused by the prisms, this cognitive knowledge was equivalent in the two cases and thus cannot explain the difference observed. Further, cognitive knowledge of the prismatic displacement has never been shown to be sufficient to abolish the adaptive aftereffect (experimenters who have worked with prisms for years will still show an aftereffect following prism exposure).
The difference observed between the ACT and the REP conditions could not be attributed to quantitative parameters such as the amount of prismatic shift or the duration and timing of feedback, as these factors were the same across the two conditions. The average magnitude of errors and the rate of correction during the exposure phase revealed near identical profiles, eliminating differences in error correction during exposure as a potential factor. The remaining critical variable appeared to be the perceived coincidence of the feedback source and the hand; only in the ACT condition, where there was a perceived physical connection between the light and the finger, did robust aftereffects consistent with perceptual recalibration occur.
It should be noted that the evaluation of the subjects' perceived
physical coincidence is an inferential one, primarily due to the
difficulty in experimentally assessing this variable in any
quantitative way. Having ruled out other potential explanations, however, a difference in how the subjects perceive the feedback remains
the most logical explanation of the data. Similar conclusions have been
drawn in studies of visual illusions resulting from vibration of the
limb (DiZio et al. 1993; Lackner and Shenker 1985
), as well as in studies of the effects of limb movement on size perception of a visual afterimage of the hand (Carey and Allan 1996
).
The precise conditions or requisite factors leading to a perceived
coincidence between the limb and the feedback source remain to be
determined. For instance, the sense of coherence may be differentially
influenced by the somatosensory input from the LED, the potential for
slight illumination of the fingertip, or the cognitive knowledge of the
LED's presence on the finger. Furthermore, the possibility exists that
the visuomotor system could be conditioned to accept a representational
signal as a compelling indicator of the actual hand position if, for
example, the subject were trained in advance with both types of
feedback concurrently, or if changes in the relationship between the
representational feedback and the limb position were made gradually
(Bock and Burghoff 1997; Kagerer et al.
1997
).
In fact, a recent study using representational feedback was able to
generate a global realignment of the visuomotor map (consistent with
perceptual recalibration) by providing both a familiarization phase
with continuous feedback of finger position, as well as a gradual
introduction of the displacement (Vetter et al. 1999). The aftereffect measures in this study, however, must be interpreted in
light of the fact that they were maintained through the postexposure phase with a "refresh exposure trial" every fourth reach. By
contrast, the aftereffects observed in the ACT condition, when the
feedback source was coincident with the hand, were relatively stable
over 50 reaches with no additional feedback provided to the subject.
It is interesting to note that a difference in aftereffect occurred
between the two conditions in spite of near-identical error correction
profiles during exposure. This suggests that, if indeed the ACT and REP
conditions elicit perceptual recalibration and visuomotor skill
acquisition, respectively, perhaps a common error correction mechanism
underlies both processes. Studies have shown that patients with
cerebellar lesions demonstrate impaired error reduction during exposure
to prisms, as well as a subsequent lack of aftereffect (Martin
et al. 1996a; Weiner et al. 1983
).
PET studies have shown activation of posterior parietal cortex during
prism adaptation under conditions where the effects of error correction
were removed (Clower et al. 1996). Recent work has also
demonstrated that parietal stroke patients with hemispatial neglect can
be therapeutically rehabilitated by brief exposures to prismatic
displacement (Rossetti et al. 1998
). Both findings
support a potential role for parietal cortex in subserving the process
of perceptual recalibration. In the monkey, the inferior parietal
cortex has been shown to receive second-order projections from the
dentate nucleus of the cerebellum, providing an anatomical route for
the potential coordination of error corrective information with the
recalibration process (West et al. 1999
).
One might speculate that the divergent processes of perceptual
recalibration and visuomotor skill acquisition are selectively employed
depending on whether the particular experimental context produces a
perceived internal or external error. Our findings are consistent with
the notion that when visuomotor discrepancies occur, feedback that is
perceived to be coincident with the limb is registered as an internal
error, leading to the induction of a perceptual recalibration; whereas
feedback that is not perceived to be physically coincident with the
limb is registered as an external error, leading to the reduction of
error during exposure but little or no apparent aftereffect. It is also
possible that the perception of the error as internal or external in
origin might lead the subject to rely preferentially on either
egocentric or allocentric cues for the guidance of movement. Studies
have shown that there is functional interaction between the two frames of reference, and that this interaction can be affected by experimental conditions (Gentilucci et al. 1996,
1997
).
Other studies have indicated that the integration of visual and
proprioceptive information can be highly sensitive with regard to
explicit vision of the hand itself, or perceived physical continuity between the hand and the source of feedback (Carey and Allan
1996; Lackner and Shenker 1985
;
Ramachandran and Rogers-Ramachandran 1996
).
Although these studies did not address adaptation per se, their results
support the notion that induction of perceptual recalibration may be
facilitated by the knowledge, or perception, of a physical coincidence
between conflicting sources of information. This concept, which has
been termed the "assumption of unity," proposes that in order for
the subject to register an internal sensory discrepancy, there must
exist a presumption that the information obtained by the different
senses (i.e., vision and proprioception) arises from a singular distal
event (Bedford 1999
; Held et al. 1966
;
Radeau and Bertelson 1977
; Welch 1972
).
Although such a condition is normally met in the physical world, representational manipulations may provide a set of circumstances where unity between the effector of the movement and the visual feedback is not necessarily presumed. This distinction has important implications in regard to studies using virtual reality environments and computer interface technology. Such tools have been embraced as a means to examine the questions of visuomotor integration and plasticity, often with the presumption that the CNS deals similarly with such artificial environments as it does with normal visually guided reaching. Our results suggest that perhaps the difference between these tasks is more than a superficial one, and that future studies are warranted to explore the issue further.
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ACKNOWLEDGMENTS |
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We thank Y. Rossetti and M. Meunier for helpful comments on a previous version of the manuscript.
This project was supported by the Human Frontier Science Program Organization.
Present address of D. M. Clower: Dept. of Neurobiology, University of Pittsburgh, Pittsburgh, PA 15260.
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FOOTNOTES |
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1
Recent work has indicated that acquisition of a
dynamic versus a kinematic "internal model" may involve separate
coordinate systems as well as distinct sensory error signals
(Flanagan et al. 1999; Krakauer et al.
1999
). Thus while kinematic rearrangements are often acquired
with a relative absence of aftereffects, it is unclear if this holds
true for dynamic rearrangements. Part of the difficulty in assessing
this factor lies in the way that aftereffects are measured. For
example, Shadmehr and colleagues have noted aftereffects from exposure
when using a task in which a transforming force field is applied to a
manipulandum to induce acquisition of a new dynamic internal model
(Shadmehr and Brashers-Krug 1997
; Shadmehr and
Mussa-Ivaldi 1994
). However, these aftereffect measurements
were obtained using randomly inserted "probe trials" while the
subject was actively working within the dynamically distorted field.
Thus while the same terminology is applied, the results are not
directly comparable to the aftereffect measures observed after prism
exposure. While subjects may, after visuomotor skill acquisition,
continue to execute the task-dependent rule that they have learned,
this should not be confused with aftereffects occurring when subjects
knowledgeably attempt to operate under the original visuomotor
arrangement. Aftereffects resulting from perceptual recalibration occur
in spite of subjects' awareness that they have returned to the
original visuomotor arrangement
they are unable to consciously
"overrule" the new mapping they have established.
Address for reprint requests: D. Boussaoud, Institut des Sciences Cognitives, 67 Boulevard Pinel, 69675 Bron, France (E-mail: boussaoud{at}isc.cnrs.fr).
Received 2 February 2000; accepted in final form 11 July 2000.
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REFERENCES |
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