Selective Use of Perceptual Recalibration Versus Visuomotor Skill Acquisition

Dottie M. Clower1 and Driss Boussaoud2

 1Research Service (151S), Veterans Affairs Medical Center, Syracuse, New York 13210; and  2Institut des Sciences Cognitives, 69675 Bron, France


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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.


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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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Fig. 1. Physical arrangement of experimental apparatus. The subject viewed a virtual image of the target projected onto a semi-reflective mirror. In the actual feedback (ACT) condition, he received feedback of the touch position via a light attached to the index finger, which was illuminated for 200 ms at the end of each reach. The light was visible through the semi-reflective mirror (whereas the hand was not), and he could compare the location of the light-emitting diode (LED) with the image of the target. In the representational feedback (REP) condition, the subject received feedback from a computer-generated square representing the hand position. In this condition, the hand was visible through the mirror. The square superimposed the position of the finger below, and the subject compared its position with the target.

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.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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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Fig. 2. Average adaptive aftereffects for ACT and REP conditions. Values shown are the group means (n = 6), and error bars indicate SE. The shift represents the difference in visual degrees between preexposure and postexposure reaching endpoints. A positive value indicates a rightward shift.

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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Fig. 3. A: normalized results for both ACT and REP conditions during the 3 exposure phases, plotted by trial number. Within each phase, the 1st data point represents the average error for all subjects on the 1st 5 reaches. The remaining 3 points in each phase represent the average error during each subsequent group of 15 reaches. The divisions are asymmetrical to allow a focus on the initial few reaches of the exposure and postexposure periods, when potential effects are most apparent. B: time course of error reduction during prism exposure for ACT and REP conditions. Displays the average error of all subjects (n = 6) for each of the 1st 10 reaches performed during the exposure condition. Error bars indicate SE.

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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Table 1. Comparison of ACT and REP conditions during exposure

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.


    DISCUSSION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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 removed---a 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.


    ACKNOWLEDGMENTS

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.


    FOOTNOTES

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.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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