Perceptual & Motor Skills: Perception 2014, 118, 2, 491-506. © Perceptual & Motor Skills 2014

EFFECTS OF REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION ON THE SOMATOSENSORY CORTEX DURING PRISM ADAPTATION1, 2 HEE-CHUL YOON, KYUNG-HYUN LEE, DONG-CHAN HUH, AND JI-HANG LEE Sungkyunkwan University, Seoul, Republic of Korea DONG-HYUN LEE Sangmyung University, Seoul, Republic of Korea Summary.—Although the behavioral characteristics and the neural correlates of prism adaptation processes have been studied extensively, the underlying mechanism is yet to be investigated. Recently, somatosensory suppression was heralded as a mechanism for the sensory re-alignment process accompanying the adaptation. Somatosensory suppression should facilitate the re-alignment process in the proprioceptive system. The shift in the proprioceptive system takes place mostly during a concurrent visual feedback (CVF) condition; during a terminal visual feedback (TVF) condition, the visual system experiences significant adaptation (visual shift), so somatosensory suppression should have minimal functional consequences under TVF. To test this hypothesis, a repetitive transcranial magnetic stimulation (rTMS) was applied to the primary somatosensory cortex as an artificial somatosensory suppression right after the reaching initiation in CVF and TVF conditions, and changes in adaptation were observed. Because somatosensory suppression is already in effect during CVF, rTMS would cause no significant changes. During TVF with rTMS, however, significantly different patterns of adaptation could be expected when compared to a sham rTMS condition. Young adults (N = 12) participated in 4 sessions (CVF/ TVF, real/sham rTMS); visual, proprioceptive, and total shifts were measured. Movement time and curvature of the reaching movement were measured during the adaptation phase. Results showed that while the total shift was unchanged, the proprioceptive shift increased and the visual shift decreased in the TVF condition when rTMS was delivered. However, the total, proprioceptive, and visual shifts were not influenced by rTMS in the CVF condition. Suppression of proprioception induced by the rTMS could be one of the requisites for successful proprioceptive shift during prism adaptation.

From the 1950s, experimental psychologists have used the wedged prism to introduce a controllable sensory-perceptual environment where participants displayed distinctive and measurable behavioral patterns of adaptation (Held & Hein, 1958; Taylor, 1962; Harris, 1963; Held & Mikaelian, 1964). The prism adaptation paradigm allows better understanding of the Address correspondence to Ji-Hang Lee, College of Sport Science, Sungkyunkwan University, 300 Chunchun-Dong, Jangan-Gu, Suwon, Gyungki-Do, Republic of Korea or e-mail ([email protected]). 2 This work was supported by the National Research Foundation of Korea Grant, funded by the Korean Government (NRF-2011-327-G00093). 1

DOI 10.2466/24.27.PMS.118k18w5

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flexibility of human motor behavior when available sensory information from vision and proprioception cause perceptual conflicts (Cohen, 1966). When a person looks through a prism lens, her visual field shifts, but the actual position of objects in the visual field, such as an arm, remain unchanged. Therefore, as the person generates a visually guided movement, he experiences perceptual conflict due to incongruent visual and proprioceptive afferents. Such conflict initially induces movement errors. However, with repeated attempts, the visual and proprioceptive systems are re-aligned, and accurate performance is re-attained. This spatial re-alignment can be estimated by measuring the prism aftereffects, and this mechanism has been extensively studied (Redding & Wallace, 1997, 2000, 2006). Upon prism exposure, the difference between the re-afferent signal from the visual system and the feedback achieved from the movement (proprioceptive system) creates spatial misalignment. When a participant can observe the reaching hand movement and a visual target through a prism lens (concurrent visual feedback: CVF), the visual system does not experience any spatial misalignment, but the proprioceptive system detects the spatial discordance and re-aligns toward spatial agreement with the input of the visual system (the “proprioceptive shift”). In contrast, when visual feedback of the reaching motion is blocked and only the end locations of the reaching hand and target are available right after the movement (terminal visual feedback: TVF), the proprioceptive feedback causes the visual system to detect discordance. The consequent re-alignment of the visual system toward spatial agreement with the proprioceptive system (the “visual shift”) occurs. Therefore, measurement of aftereffects using shift tests can help identify the system in which realignment is occurring. The recent emergence of cognitive neuroscience has also started identifying brain areas associated with the perceptual re-alignment processes accompanying prism adaptation. The results of previous studies appear to agree that prism adaptation takes place through perceptual re-alignment processes in the cerebellum (Baizer, Kralj-Hans, & Glickstein, 1999; Morton & Bastian, 2004; Luaté, Schwartz, Rossetti, Spiridon, Rode, Boisson, et al., 2009), while neural activities in the posterior parietal cortex (Inoue, Kawashima, Satoh, Kinomura, Sugiura, Goto, et al., 2000) and the premotor area (Kurata & Hoshi, 1999) were shown to be correlated with an error-correction mechanism, distinct from the re-alignment process, during the adaptation process (Clower, Hoffman, Votaw, Faber, & Wood, 1996; Lee & van Donkelaar, 2006; Newport, Brown, Husain, Mort, & Jackson, 2006; Newport & Jackson, 2006). However, few empirical studies have addressed the underlying neural mechanism of the spatial re-alignment process. Current understanding of the prism adaptation allows identification of the characteris-

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tics of behavioral processes and neural correlates, but does not specify how the neural structures carry out their hypothesized functions. Recent studies have reported that when the spatial misalignment is detected in the proprioceptive system during the adaptation process, the central nervous system suppresses the proprioceptive afferents, providing the opportunity for re-alignment. During this mechanism of somatosensory suppression, the re-afferent signal becomes attenuated during the voluntary arm-reaching movement (Rushton, Rothwell, & Craggs, 1981). The psychophysical characteristics of the somatosensory suppression/gaiting mechanism have been well documented (Angel & Malenka, 1982; Milne, Aniss, Kay, & Gandevia, 1988; Blakemore, Wolpert, & Frith, 1998), and the neural correlates of this mechanism have been recently suggested (Seki & Fetz, 2012). Because re-afferent (proprioceptive) feedback from the moving arm is the major source of spatial discordance under CVF in the prism-adaptation paradigm, it could be assumed that the somatosensory suppression may function as an executive mechanism for proprioceptive-shift adaptation. A few clinical studies have reported successful adaptation of de-afferented patients (Bard, Fleury, Teasdale, Paillard, & Nougier, 1995; Ingram, van Donkelaar, Cole, Vercher, Gauthier, & Miall, 2000). Further, more direct evidence for the involvement of a proprioceptive-suppression mechanism during sensory motor adaptation can be inferred from Jones, Wessberg, and Valbo (2001), who measured feedback-related muscle spindle activity from the arm during visuomotor adaptation and reported the attenuation of re-afferent firing rates. Balslev, Christensen, Lee, Law, Paulson, and Miall (2004) showed that suppression of proprioceptive feedback actually enhanced the accuracy of the response while the participant experienced perceptual conflicts. While these previous studies demonstrated the possible involvement of somatosensory suppression mechanisms in sensory motor adaptation, the direct link between the somatosensory suppression and the spatial re-alignment process (known to be the underlying mechanism of prism adaptation) has not been investigated. In this study, a short train (500 msec.) of high-frequency (10 Hz) repetitive transcranial magnetic stimulation (rTMS) pulses (analogous to five single pulses of TMS separated by 100 msec.) was applied to the primary somatosensory cortex to create an artificial form of somatosensory suppression during prism adaptation. The effect of a 10 Hz, 500 msec. rTMS pulse on the somatosensory cortex has not been directly addressed. However, previous studies using a similar protocol (a short train of 10 Hz rTMS pulses) showed significant temporary (~1000 msec.) inhibitory effects on various cortical structures, including the posterior parietal cortex (Vesia, Prime, Yan, Sergio, & Crawford, 2010), the middle temporal area (Dessing, Vesia, & Crawford, 2013), the dorsolateral prefrontal cortex (Hamidi,

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Tononi, & Postle, 2009), the intraparietal sulcus (Hamidi, Tononi, & Postle, 2008), and the prefrontal cortex (Rossi, Pasqualetti, Zito, Vecchio, Cappa, Miniussi, et al., 2006). Disruptive effects of TMS can be observed in specific tasks over virtually all cortical sites, including prefrontal, parietal, temporal, or occipital cortices (Jahanshahi & Rothwell, 2000). Also, over the somatosensory cortex, rTMS has been shown to interfere with somatosensory processing in a behaviorally relevant way (Knecht, Ellger, Breitenstein, Bernd Ringelstein, & Henningsen, 2003; Azañón & Haggard, 2009; Jacobs, Premji, & Nelson, 2012). Thus, it is expected that the rTMS protocol used in this study will be inhibitory. Further, because most sensory afferents are delivered to and processed in the somatosensory cortex, the inhibition of this region would create, in theory, some loss of that function (Balslev, et al., 2004). The pattern of prism adaptation differs depending upon the type of visual environment. Perceptual re-alignment takes place in the sensorimotor system where the perceptual conflict is experienced. As discussed previously, when a participant can observe his hand during a reaching movement (CVF) with the prism on, the proprioceptive shift is the dominant process for detection of discordance and consequent re-alignment. On the other hand, when a participant can only see the end result after the reaching movement is completed (TVF), then the visual system experiences the discordance and the amount of proprioceptive re-alignment is minimal (Redding & Wallace, 1997). Because the changes in the proprioceptive system are required only during CVF, it could be hypothesized that somatosensory suppression would take place during only that condition. In contrast, during TVF, updating of the mapping would mostly take place in the visual system, and therefore somatosensory suppression may not have much functional consequence. The purpose of this study was to provide evidence that the somatosensory suppression is a mechanism facilitating the proprioceptive shift for spatial re-alignment during prism adaptation. By introducing artificial proprioceptive suppression using the rTMS technique, the amount of visual, proprioceptive, and total shifts were measured and compared in two different visual feedback conditions. Hypothesis 1. When the inhibitory rTMS is delivered on the somatosensory cortex under CVF, no noticeable effects are expected because the proprioceptive system is already suppressed in this feedback condition. Hypothesis 2. When the inhibitory rTMS is delivered on the somatosensory cortex under TVF, proprioceptive afferents should be disrupted by the artificial somatosensory suppression, reducing visual shift and increasing proprioceptive shift.

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METHOD Participants Participants were 12 young (M age = 27 yr., SD = 4.9) and healthy righthanded adults with normal vision. None of the participants had a history of neurological disease or seizure. All participants provided written informed consent before the commencement of the experiment after a briefing regarding the procedures and possible risks. Each participated in four experimental sessions separated by at least 14 days and received an honorarium upon completion. The study was approved by the local ethics committee and was performed in accordance with the 1964 Declaration of Helsinki. Experimental Setup Each participant was seated in a chair with his hands on a table at chest height. There was a small marker on the table indicating the hand resting position (right in front of the participant’s midline) so that he could identify its location by cutaneous sensation without having to look down. The visual target was projected with a beam projector onto a semi-silvered mirror located at the neck level. There was also an LED lighting system under the mirror. With this light on, participants could see the hand movement under the mirror and the visual target on the mirror at the same time. With the light off, visual information regarding the hand’s position was not available, and only the target on the mirror was visible. The light was controlled by a pressure sensor (a generic force transducer) attached to the tip of the index finger. In the CVF condition, the light was turned on as the finger left the starting position and was turned off 500 msec. after the reaching movement was completed so participants could observe their reaching movement. In the TVF condition, the light was turned on as the pressure sensor on the finger touched the table upon completion of reaching movement and remained on for 500 msec. (Lee & van Donkelaar, 2006). Target display, inputs from the pressure sensor, and LED light control were handled using the SuperLab software (Version 2.0, Cedrus, San Pedro, CA, USA). To introduce visual distortion, a 20-diopter press-on prism sheet (3M, St. Paul, MN, USA) was attached to the right side of a working goggles lens (shifting the visual field to the left), and the rest of the goggles (including the left lens) was covered with opaque paint. While comfortably seated, the participant’s head was immobilized by an adjustable chin rest. Therefore, while wearing the prism goggles, the field of view included the target location and the area required for the reaching movement, but the view of the starting position was blocked. The participant was asked to visually fixate on the target as it appeared on the mirror. Kinematic data (including the final location) of the fingertip during the reaching move-

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ment and the pre- and post-prism shift tests were recorded using a Liberty motion analysis system (Polhemus, Colchester, VT, USA). A Rapid 2 (The Magstim Company, Whitland, UK) system was used to deliver transcranial magnetic stimulation to the somatosensory cortex. Measures Reaching errors (mediolateral distance between reached point and target) and movement time were measured during adaptation. Movement errors to the left were considered negative while those to the right were positive. Also, movement curvature was measured as an index of the extent of on-line error correction. It was calculated as the ratio between the total reaching displacement and the distance between the starting and ending position of the sensor attached to the index finger. A perfectly straight finger trajectory would have a ratio score of 1.0. Because the movement curvature becomes almost identical after several attempts upon prism exposure, only data from the initial five reaching movements in each session were averaged for comparison. The major dependent variables were visual, proprioceptive, and total shifts. In the total shift test, the participant made 10 pointing movements without visual feedback from the hand to a visual target positioned straight ahead of the starting position. In the proprioceptive shift test, the participant pointed 10 times without vision of the hand or target to a position they perceived to be straight ahead. For these tests, the participant was asked to make a very slow movement. Corrective or exploratory hand movements were encouraged too. In the visual shift test, a target appeared 30 cm left or right of straight ahead and moved toward the center of the display at 10 cm/sec. The participant was asked to track the target motion with his eyes and was required to press the transducer attached to the index finger tip when he perceived the target to be straight ahead. The changes induced by the prism adaptation were monitored by calculating the mediolateral difference (cm) in the total, proprioceptive, and visual shift tests between the pre- and post-adaptation periods. Procedure The parameters for rTMS stimulation were identified before each session, including the location of the primary somatosensory cortex and the intensity of the stimulation. Participants were seated in a comfortable chair and were instructed to keep their eyes closed and to relax. The primary motor cortex location responsible for the contraction of the first dorsal interrosseous (FDI) muscle (motor hot spot) was identified by observing TMS-elicited electromyography (EMG) responses. As a starting point, stimulation was delivered to the midpoint of the vertex-preauricular line using the international 10–20 system, and the site of stimulation was then

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systematically moved until the motor hotspot was located. Observing signals from the EMG electrode attached to the right-hand FDI muscle, the location of the motor hot spot was confirmed by identifying the stimulation area where the maximum EMG response was observed with the minimum TMS intensity (stimulation threshold). By moving the stimulation coil 2.5 cm posterior from the motor hot spot, it was possible to identify the stimulation site for the somatosensory cortex and calculate stimulation intensity (110% of the stimulation threshold) based on protocols from previous studies (Balslev, et al., 2004). Before the experiment, participants practiced several reaching movements while wearing the one-eyed (right side) goggles without a prism lens. The starting and target positions were recorded during this period. For the pre-adaptation (baseline) trials, participants performed 10 proprioceptive, 10 visual, and 10 total shift tests in a pseudo-randomized order. Immediately following the pre-adaptation trials, participants switched to the prism goggles with their eyes closed. Then, under the given visual condition (CVF or TVF), participants opened their eyes and performed a reaching/pointing movement toward the visual target 40 times (prism-on trials). While participants were asked to make movements at a comfortable pace, a fast speed (approximately no slower than 1000 msec. as previously practiced without the prism) was encouraged. The 10 Hz, 500 msec. rTMS pulse was delivered at the initiation phase of the movement as the reaching hand left the starting point (signaled by the force transducer on the fingertip). The effect of rTMS during each reaching trial is known to be shortlived (less than 1000 msec.). Because participants' average movement times were no greater than 600 msec., the effect of rTMS would be long enough to cover the whole trial duration. There was a 7 sec. intertrial interval between each reaching movement. Any possible washout problem by repeatedly turning the light on and off could be prevented by this intertrial interval. During the real rTMS condition, the coil was positioned tangential to the scalp, and the handle was oriented at 45˚ to the parasagittal plane. During the sham TMS, the coil was tilted at 90˚ to the scalp so that one wing of the coil was in contact with the scalp over the site of stimulation. This sham TMS coil arrangement reproduced the sound of real rTMS with minimal effects on the cortex. Upon completion of the prism-on trials, participants changed back to normal goggles and again performed the visual, proprioceptive, and total shift tests (post-adaptation trials). The order of four data collection sessions was pseudo-randomized across participants. Analysis The shift test results (from the pre- and post-adaptation trials) and the kinematic data (from the prism-on trials) were stored in the Liberty system and transferred to MATLAB (Version 7.8, MathWorks, Natick,

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MA, USA) software for further analysis. The purpose of measuring movement error during prism-on trials was to provide descriptive patterns of adaptation. Therefore, only the results of shift tests, movement time, and the movement curvature were compared between the real TMS and sham TMS conditions in the two visual feedback conditions in a two-way repeated-measures analysis of variance (ANOVA). RESULTS Figure 1 and Table 1 show the group average for movement error across 40 movements made during the prism-on phase in each session. In each case, the initial trials displayed large errors in the direction induced by the prism, which were gradually reduced to near zero with repeated attempts. 0

Target

–2 –3

Leftward Error

Reaching Error (cm)

–1

–4 –5 –6 0

5

10

15

20

25

30

35

40

Prism-on Reaching Trials FIG. 1. Means and standard deviations of reaching movement error scores during the prism-on period. The black symbols represent the sham rTMS condition, and the white symbols represent the real rTMS condition. Circles represent CVF and triangles TVF.

Movement curvature (displacement-to-target distance ratio) analysis indicates the amount of on-line correction occurring during the initial phases of the adaptation (the first five reaches). Table 1 shows the significant main effect of the visual feedback condition. Movement curvature during the CVF condition was significantly greater than during the TVF condition. However, the main effect of rTMS conditions (real vs sham) and the interaction of the visual feedback condition and rTMS condition were not significant (Fig. 2A). Lack of a significant interaction indicates that there was no significant effect of rTMS in either feedback condition. The significantly large movement curvature in the CVF condition was as expected

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PRISM ADAPTATION TABLE 1 ANALYSES OF VARIANCE FOR EFFECTS OF FEEDBACK AND RTMS CONDITIONS ON MOVEMENT CURVATURE AND TIME, AND VISUAL, PROPRIOCEPTIVE, AND TOTAL SHIFT Measure Movement curvature Movement time

Source

MS

rTMS (T)

0.005

Visual feedback (F)

0.81

44.11

T×F

0.02

0.69

rTMS (T) Visual feedback (F) T×F

Visual shift

rTMS (T) Visual feedback (F) T×F

Proprioceptive rTMS (T) shift Visual feedback (F) T×F Total shift

F1, 11

rTMS (T) Visual feedback (F) T×F

0.001

p

η2

.98

0.005

< .001 0.80 .42

Post hoc Comparisons CVF > TVF

0.06

517.09

0.20

.67

0.02

2703.55

0.70

.42

0.06

25,099.07

3.93

.07

0.26

1065.01

2.31

.16

0.17

2.20

0.01

.95

0.005

758.34

9.01

< .05

0.45

TVF (sham < rTMS)

522.77

7.46

< .05

0.40

Sham < rTMS

2606.24

5.27

< .05

0.32

CVF > TVF

1219.78

12.50

345.36

1.53

3427.51

14.13

53.66

0.43

< .005 0.53 .24

0.12

< .005 0.56 .53

TVF (sham < rTMS) CVF > TVF

0.04

because of the available visual feedback during the reaching movement in this condition. In addition, the average movement time during the adaptation phases showed no significant main effect of visual feedback condition or rTMS condition. The interaction also was not significant (Fig. 2B). B

2.0

Movement Time (msec.)

Movement Curvature

A

1.8

1.6

1.4

1.2

800

600

400

200

0

1.0

CVF

TVF

CVF

TVF

FIG. 2. Means and standard deviations of movement curvature (A) and movement time (B) during the prism-on period in sham (black bars) and real (gray bars) rTMS conditions.

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B

Visual Shift (cm)

6

RealrTMS

4

2

0

C

6

6

Total Shift (cm)

Sham rTMS

Proprioceptive Shift (cm)

A

4

2

0

CVF

TVF

4

2

0

CVF

TVF

CVF

TVF

FIG. 3. Means and standard deviations of visual shift (A), proprioceptive shift (B), and total shift (C) test results under continuous (CVF) and terminal (TVF) visual feedback in sham (black bars) and real (gray bars) rTMS conditions. Asterisks indicate significant difference across conditions, p < .05.

Figure 3 shows the comparisons of total, proprioceptive, and visual shifts between sham and real rTMS conditions in two visual feedback conditions. In the case of the visual shift (Fig. 3A), no significant main effect was reported either for the visual feedback condition or rTMS condition. However, a significant interaction was observed. In proprioceptive shift tests (Fig. 3B), the effects of the visual feedback condition, rTMS condition, and their interaction were all significant. In the rTMS condition, the visual shift significantly decreased under TVF. In contrast, there was an increase of the proprioceptive shift under TVF. This presumably reflected the effect of rTMS as hypothesized. Finally, the total shift result showed a significant main effect of the visual feedback condition, while the effect of the rTMS condition and their interaction were not significant (Fig. 3C). Because the total shift requires the involvement of both visual and proprioceptive systems, any possible changes elicited by rTMS might have been compensated as discussed above. The significant main effect of the visual condition reflects the inherent differences in the tasks used in this study. The amount of feedback is greater during CVF (in theory), as the participant can observe both the reaching movement and the terminal result. Thus, the total amount of adaptation should be greater when compared to the TVF condition. This adaptation tendency accompanying the natural reaching movement has been reported elsewhere (Lee & van Donkelaar, 2006). DISCUSSION The effects of repeated transcranial magnetic stimulation (rTMS) on the somatosensory cortex during prism adaptation were assessed. Changes in movement error during the prism-on period replicated typical ad-

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aptation patterns (Fig. 1). From the movement time and the movement curvature data, no effect of rTMS was observed in either visual feedback condition (Fig. 2, Table 1). However, the different reaching response patterns between visual feedback conditions were supported by the analysis of movement curvature results (Fig. 2A; Redding & Wallace, 2003; Lee & van Donkelaar, 2006). During the initial stage of the prism exposure, participants seemed to use the visually guided on-line correction strategy under concurrent visual feedback (CVF); in contrast, the movement curvature under terminal visual feedback (TVF) resulted in relatively straight reaching movements. Average movement time analysis, however, did not show any difference between the two visual feedback conditions (Fig. 2B). Theoretically, the on-line correction during reaching may require longer movement times. But the curved movement with greater movement time might have rapidly decreased and become straight after only a few attempts. Therefore, it could be inferred that in spite of the initial differences in reaching movement patterns, the overall characteristics of the adaptation pattern between visual feedback conditions were similar and did not show any effect of rTMS. Because rTMS was used to tap into the realignment process (after effects) of the prism adaptation only, the lack of an effect for rTMS during the prism exposure (direct effects) would not be surprising. rTMS on the posterior parietal cortex or premotor cortex (known to be involved with the error correction during the prism adaptation) might have triggered the changes in the direct effect during the prism exposure. During the prism adaptation process, detection of spatial misalignment requires the spatial coordinates of visual perception to be compared with the feedback signal from the proprioceptive system. Because these two sensory coordinate systems are not in spatial alignment upon prism exposure, the expected (visual system) coordinate is different from the achieved (proprioceptive system) coordinate. Such spatial discordance signals create misalignment, and consequently, re-alignments (shifts) take place. Changes in the proportion of visual and proprioceptive shifts to the absolute amount of total shift are indicative of the nature of the adaptation (Redding, Rossetti, & Wallace, 2005). Based on the results of previous studies, visual and proprioceptive shifts should be smaller than the total shift (Redding & Wallace, 1997). Further, the relative contribution (or amount) of proprioceptive shift to the amount of total shift is significantly smaller under TVF because most of the re-alignment in this condition takes place in the visual system (visual shift). In contrast, the amount of visual shift to that of total shift is significantly smaller under CVF because most of the re-alignment in this condition takes place in the proprioceptive system (proprioceptive shift). The general trend of results in the current study is congruent with previous findings (Fig. 3). In the control (sham)

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conditions under CVF, the proportions of proprioceptive shift to total shift were 72% (3.26 vs 4.56 cm), while the proportion of visual shift was 28% (1.28 vs 4.56 cm). In contrast, under TVF the proportion of proprioceptive shift to total shift was 25% (0.7 vs 3.08 cm), and the proportion of visual shift to total shift was 69% (2.11 vs 3.08 cm). The effects of rTMS during the prism adaptation could be observed in the analysis of after effects. The basic assumption about rTMS application is its functional inhibitory influence on proprioceptive perception when delivered to the somatosensory cortex (for a review, see Azañón & Haggard, 2009; Vidoni, Acerra, Dao, Meehan, & Boyd, 2010; Jacobs, et al., 2012). However, the exact nature of changes in the proprioceptive afferent induced by rTMS is speculative. The proprioceptive afferents could have been distorted, inhibited or otherwise at the somatosensory cortex level by rTMS. However, we have assumed that such changes would have a functional consequence of the “suppression-like” effect. Also, possible spread of rTMS over the adjunct areas such as the primary motor cortex or the posterior parietal cortex could have influenced the results. This possibility was not directly tested. However, the effect of inhibitory rTMS on the stimulation site was shown to have distinctive somatosensory suppression effect when compared to the primary motor cortex and the posterior parietal cortex (Balslev, et al., 2004). Thus, one could assume the primary effect of rTMS used in this study was well-contained within the area of interest. The key dependent variable of the study was changes in proprioceptive and visual shifts under different visual feedback conditions. Specifically, increase of the proprioceptive shift and the decrease of the visual shift were expected only during the TVF condition, and the results confirmed this hypothesis. With the application of the rTMS, the amount of visual and proprioceptive shift changed only in the TVF condition. In the CVF condition with rTMS, the amount of proprioceptive shift was 2.91 cm and visual shift was 1.13 cm (total shift 4.23 cm), which is not significantly different from the sham condition (proprioceptive shift 3.26 cm, visual shift 1.28 cm). On the other hand, the amount of the visual shift significantly decreased with rTMS application from 2.11 cm to 0.37 cm in the TVF condition. Also, the effect of rTMS significantly increased the proprioceptive shift from 0.78 to 2.45 cm in this condition. In other words, there was a significant increase in the proprioceptive shift and a significant decrease in the visual shift only when the rTMS was applied during the TVF condition. In addition, results showed no significant effect of the rTMS on total shift under either visual feedback condition (Fig. 3). This suggests that participants were able to adapt despite the influence of the rTMS. According to the previous lesion or patient studies, disruption of

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brain regions such as the premotor cortex (Kurata & Hoshi, 1999) or the cerebellum (Martin, Keating, Goodkin, Bastian, & Thach, 1996) successfully inhibited adaptation. While these brain areas are involved with the re-alignment process itself, the somatosensory suppression carried out by the somatosensory cortex could be a pre-requisite for such re-alignment process. Therefore, disruption of the somatosensory cortex might not be able to completely inhibit the final adaptation. The assumption about the effect of rTMS was based on Balslev, et al. (2004), who observed an improvement of performance in a mirror-tracing task after the rTMS on the somatosensory cortex. Whatever the exact mechanism of “inhibitory” or “suppression-like” rTMS on the somatosensory cortex, the task’s inherent sensory-motor conflict was better resolved in their study under rTMS. This result supports the hypothesis that when the accuracy of the somatosensation is compromised, adaptation can benefit from a reduction of this information. Bernier, Burle, Vidal, Hasbroucq, and Blouin (2009) showed that the cortical suppression of proprioceptive afferent is a mechanism for resolving sensory-motor discrepancies. If the rTMS were simply distorting the proprioceptive signals, the proprioceptive shift would not “increase” during the TVF condition, as such an increase is indicative of a coherent suppression mechanism. Therefore, assuming the functional consequence of rTMS on the somatosensory cortex to be a “suppression-like” effect, the observed significant increase of the proprioceptive shift in the current study also implies this effect of rTMS. In conclusion, the significant increase of proprioceptive shift under terminal visual feedback, where its contribution is typically minimal, and the decrease of the typically dominant visual shift support the hypothesized changes in the adaptation mechanism facilitated by rTMS on the somatosensory cortex in a manner specific to the visual feedback condition. In this study, there was evidence that the application of rTMS on the somatosensory cortex had a proprioceptive suppression effect only during the terminal visual feedback condition; this result provides support for the hypothesis that prism adaptation entails proprioceptive suppression. These findings imply that proprioception may have limited contribution to adaptation. Further, the adaptation could be improved by reducing the proprioceptive inflow or the activity of the somatosensory cortex. Due to the complex nature of the prism adaptation process, proprioceptive suppression cannot be the only underlying mechanism. Therefore, the question of whether changes in visual perception entail a similar suppression mechanism (Redding, Rossetti, & Wallace, 2005) remains unanswered. REFERENCES

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