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Kinesthetic illusory feeling induced by a finger movement movie effects on corticomotor excitability
Neuroscience 149 (2007) 976 –984
KINESTHETIC ILLUSORY FEELING INDUCED BY A FINGER MOVEMENT MOVIE EFFECTS ON CORTICOMOTOR EXCITABILITY F. KANEKO,a* T. YASOJIMAa AND T. KIZUKAb
our visual stimulus method in the present study. The method of visual stimulus presentation was a movie in which someone else’s limb (an index finger in the present study) is moving. The computer screen on which the movie played was installed on an appropriate portion of the subject’s forearm, so that the performer’s hand appears as if it were the subject’s hand. The objective of our study was to clarify whether an illusion originating from visual input affects cortical level excitability: that is to say, whether a “sensory” illusion induced by this novel approach has a measurable “motor” effect. Since perceptual-to-motor transformation during tendon vibration was demonstrated by motor unit activity recording from an antagonist muscle of the vibrated muscle (Calvin-Figuiere et al., 1999, 2000; Romaiguere et al., 2005), if a similar effect were to be found in our experimental visual stimulus, it may be useful to provide a facilitatory effect to the corticomotor pathways corresponding to rehabilitation of patients with motor disorders of some kind. Many experimental results stress a prevalent role of vision over other senses in self-recognition, though it is largely context-dependent: we feel our hand where we see it, not the converse (Jeannerod, 2003). Various studies have concurred upon an understanding of the dominance of visual afferent information with respect to awareness of somatosensory information, and also that such information influences corticomotor excitability. The induction of a kinesthetic illusory sensation by moving visual stimulus of ambient circumstances surrounding a subject’s static hand was reported by Tardy-Gervet et al. (1982, 1984). Furthermore, it was shown that a kinesthetic illusion could be induced in arm-amputees by their observing a motion executed by the opposite, intact hand in a mirror. Ramachandran and Rogers-Ramachandran (1996) reported that most of the amputees who participated in the experiment felt an emerging, vivid kinesthetic sensation of the phantom movement in the mirror. The condition in the present study by which a movie is presented, is based on another kind of knowledge, that is, the evidence about the dominance of vision with respect to body image recognition that is associated with having somatosensory information (Botvinick et al., 1998; van den Bos and Jeannerod, 2002). The necessary condition is for there to be a precise alignment between the subject’s actual body and the performer’s body in the display. The condition settings adopted in the present study are basically different from those used in previous studies. The body observed by the subject is that of someone else; there is no voluntary action on the contralateral side during the observation; the observed person’s hand faces away from the subject, and the observed
a
Institute for Human Science and Biomedical Engineering, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba City, Ibaraki 305-8566, Japan
b
Graduate School of Comprehensive Human Sciences, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba City, Ibaraki 305-8574, Japan
Abstract—The present study aimed to clarify whether a kinesthetic illusion arises in our experimental condition (visual stimulus) and whether corticomotor excitability changes in parallel with the kinesthetic illusion. The visual stimulus was a movie in which someone else’s limb was being moved. The computer screen showing the movie was installed at an appropriate portion of the subject’s forearm, so that the performer’s hand appeared as if it were the subject’s hand (illusion). The experience of kinesthetic illusion under this condition was verified by interview using a visual analog scale. Healthy male subjects participated in this experiment. Transcranial magnetic stimulation was applied to induce motorevoked potential (MEP) from the first dorsal interosseous and abductor digiti minimi muscle. Each subject was instructed to watch the same computer display shown as in the illusion, with his own stationary hand in full view (non-illusion) and to watch a display of non-biological movement (moving text) (sham) as the control conditions. The present results showed significant facilitation of MEP under the illusion compared with the control conditions for the index finger abducting in the movie, although not for adducting. MEP in the abductor digiti minimi showed no change during either abduction or adduction of the little finger. The present study demonstrated that an illusion of self-motion can be created by a video of a moving abstract index finger, and inputs to the corticomotor pathways during the self-motion illusion facilitated the corticomotor excitability. The excitatory effect of the illusion depended on the movement direction of the index finger. © 2007 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: kinesthesia, illusion, transcranial magnetic stimulation, motor-evoked potential, mirror neuron system.
It has been found that kinesthetic illusions of limb movement induced by tendon vibration against the muscle spindle alter sensorimotor cortex excitability with the reception of sensory afferent input, despite the fact that the vibrated limb remains immobile (Naito et al., 1999, 2002, 2005, 2006; Calvin-Figuiere et al., 1999, 2000; Romaiguere et al., 2003, 2005; Naito, 2004; Naito and Ehrsson, 2001, 2006; Casini et al., 2006). We investigate whether a kinesthetic illusory sensation could be induced in a subject by *Corresponding author. Tel: ⫹81-29-861-7885; fax: ⫹81-29-861-6660. E-mail address: [email protected] (F. Kaneko). Abbreviations: ANOVA, analysis of variance; EMG, electromyography; MEP, motor-evoked potential; TMS, transcranial magnetic stimulation; VAS, visual analog scale.
0306-4522/07$30.00⫹0.00 © 2007 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2007.07.028
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object is a computer display (not a mirror or an actual body). First, the aim of the present study was to clarify whether the kinesthetic illusion arises in our experimental condition. Second, we tested an input originating from the self-movement illusion affecting the corticomotor excitability in parallel with the kinesthetic illusion during that condition.
EXPERIMENTAL PROCEDURES Experiment 1 Subjects. Twenty neurologically healthy male subjects (age 21–31 years) participated in this experiment. All subjects were self-declared right-hand dominant. Each gave his informed consent for the experiment, which was approved by the local ethics committee. The subjects were divided into Group A and Group B. Ten subjects (Group A) underwent the resting, illusion, and nonillusion conditions, and the other 10 subjects (Group B) underwent the resting, illusion, and sham conditions. The groups were divided this way because the number of transcranial magnetic stimulations (TMS) subjects might undergo would be over the limit established by the local ethics committee if all four conditions were employed on each subject. Electromyography (EMG) recording and TMS. Surface EMG signals were recorded from the first dorsal interosseous muscle and from the abductor digiti minimi muscle of the left side using bipolar surface electrodes. The Ag–AgCl disc electrodes (5 mm in diameter) were arranged at 10 mm intervals. Before the electrodes were attached, the skin area was rubbed with alcohol and abraded with abrasive skin-prepping gel. EMG signals were amplified (Neuropack MEB-2200, Nihonkoden Co. Ltd., Toyko, Japan) at an appropriate level (⫻1000) and filtered (5.3–1000 Hz). The EMG signal, a trigger signal to be carried to the transcranial magnetic stimulator (Magstim 200, The Magstim Co. Ltd., Wales, UK), and the output signal of the stimulation from the Magstim 200 were digitized at 20 kHz per channel by a CED 1401 (Cambridge Electronic Design Limited, Cambridge, UK) using a personal computer. A round coil with a 9-cm outside diameter was used to elicit motor-evoked potential (MEP) both from the single target muscle, which is the agonist muscle of the index finger movement, and from a control muscle (the abductor digiti minimi) close to the first dorsal interosseous. For each condition TMS was applied to induce MEP and was delivered through a round coil placed so that the A or B side faced up (RdA or RdB) around Cz. MEP was obtained in accordance with a report of the International Federation of Clinical Neurophysiology (Rossini et al., 1994; Rothwell et al., 1999). TMS was applied during the resting condition before the other three conditions. MEP was recorded from the first dorsal interosseous and abductor digiti minimi. The resting motor thresholds were defined as the minimal intensity capable of inducing MEP with a peak-to-peak amplitude greater than 50 V in both coils in at least four out of seven trials. During testing, the TMS stimulus intensity capable of inducing MEP with peak-to-peak average amplitudes of 0.5–1 mV during the resting condition was also used in the other three conditions. As a result, TMS was delivered at 114.61⫾7.91% (mean⫾S.D.) of the subjects’ resting motor threshold in all trials. MEPs were induced at least 10 times for each condition. The EMGs, which were shown on a computer display (17 inches), were monitored by more than two experimenters in all of the stimulations with a 500 V scale per division (a total of 10 divisions for each muscle); the experimenters were required to reject the trial if tiny muscle activation was recognized during testing. Furthermore, the absence of EMG activation during each test was visually reconfirmed offline after the experiments.
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Supramaximal M-waves were recorded by applying an electrical current to the ulnar nerve from both the first dorsal interosseous and abductor digiti minimi after TMS testing. The current intensity was gradually increased, and the peak amplitude of the M-wave was visually confirmed. The amplitudes from the MEP of both the first dorsal interosseous and abductor digiti minimi were normalized individually with the supramaximal M-wave amplitude. Procedures. During the experiment, the subject sat in a comfortable chair with his left hand on a custom-built experimental table. Comfortable positions for the joints were established depending on each subject in such a way that the shoulder joint was set at almost 45° abduction and flexion, and the elbow joint was positioned at about 30° flexion. The condition of the first experimental block was the resting condition, in which the TMS was applied before then being applied to the other conditions in random order. The order for RdA vs. RdB was randomized for the subjects. Two kinds of control conditions (“non-illusion” and “sham”) against the illusion condition were adopted to compare the illusory effect on corticomotor pathways. In the next experimental block, the resting condition was followed randomly by either RdA and RdB in the following three conditions. In the illusion condition, a computer screen showing the abduction of someone else’s index finger was placed on the subject’s left side distal forearm. The position of the screen was adjusted so that the subject would see the action on the screen as if watching his own index finger moving (Fig. 1A). While the screen was being pre-set, the subject was interviewed to confirm whether the adjustment of its position was appropriate to induce a kinesthetic illusion. Fig. 1B illustrates how the performer’s index finger was passively moved by our experimental device in the movie presented on the screen. In the non-illusion condition, the subject was instructed to watch the same computer screen showing the abduction of someone else’s index finger, only the subject could recognize that his own finger was not moving since his own static hand was in his field of view (Fig. 1C). In the sham condition, the subject was shown white 3D text (“Microsoft Windows”) on the black computer screen, running from left to right with rotating in the side direction. This was the screen saver function of Microsoft Windows XP. This particular text was chosen as being unlikely to induce imagery relating to body movement. Visual stimulus of someone else’s hand action. In this study, a specialized visual feedback condition was formulated for future clinical applications of kinesthetic illusion. The movie had been made prior to the experiment. The performer, who did not participate in the TMS experiment, sat in a comfortable chair with his left hand on a custom-built experimental table in the same manner as in the TMS experiment while the movie was made. This performer’s body physique and skin color were easily recognizable as those of an average Japanese man. A consumer-type digital video camera (HDR-HC1, Sony Style (Japan) Inc., Tokyo, Japan) was carefully positioned beside the performer’s face at eye level so that the camera angle would be the same as the angle of the eyes in regard to the index finger movement. The angle between performer’s index finger and thumb was set at 80° in their initial positions. The movement axis of the index finger’s abduction/adduction was positioned on the servomotor’s axis built in to the device (Fig. 1B). The motion of the digit saucer, in which index finger was placed, was controlled by personal computer. At the start of the movie, the index finger was adducted and in contact with the middle finger. The passive abduction took 3 s, and the 3-s adduction of the index finger made an entire “round” lasting 6 s. In both the illusion and non-illusion conditions, the computer screen on which the movie played was installed on an appropriate portion of the subject’s forearm. The movie (QuickTime ver. 7.1.3, Apple Computer, Inc., CA, USA) window in the display was adapted to the subject’s body size by changing the window size so that the presentation of the performer’s hand could be adjusted to the
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Fig. 1. Three conditions in experiment 1 (A–D) and an additional condition performed in experiment 2 (E) are shown. Illusion: A computer screen showing the abduction of someone else’s index finger was placed on the subject’s distal forearm. The position of the screen was adjusted accurately so that the subject would see the action on the screen as if watching his own index finger moving (Fig. 1A). Fig. 1B illustrates the hand setting and index finger movement in the movie. The index finger was passively moved by an experimental device; one “round” of abduction and adduction took a total of 6 s. Non-illusion: Subject was instructed to watch a computer screen showing the abduction of someone else’s index finger, as in the illusion condition. The difference between the illusion and non-illusion conditions was that, in the latter condition, the subject could recognize that his own finger was not moving because his own static hand remained in his field of view (Fig. 1C). Sham: Subject was shown white 3D text moving on the black background of the computer screen, which was set up in the same position as in the illusion condition (Fig. 1D). In experiment 2, a movie of the little finger being moved (abduction and adduction) was added as a control condition. The little finger of the left hand was set on the digit saucer in the conditions little-abd and little-add.
subject’s hand size. TMS was applied at the point when the index finger in the movie was in the middle position of its abduction movement range once every two or three rounds. This stimulus timing was one of the important points, since it was elucidated that the motor excitability during the observation of a certain action changes depending on a cyclic time course (Borroni et al., 2005; Montagna et al., 2005). For the illusion and non-illusion conditions, the subject’s actual index finger was statically held on the experimental table in a 30° degree abduction position to the middle finger and the subject was directed to rest it there throughout the testing conditions. Evaluation of introspection. A visual analog scale (VAS) was adopted to evaluate the introspective perception in the
illusion condition (Scott and Huskisson, 1976). Subjects were interviewed concerning how strongly they experienced the introspective perception associated with the kinesthetic sense of their own finger movement after the illusion condition session, so that their answer includes strength of the feeling about movement and ownership. In the present study, zero indicated that the subjects had no illusory sensation at all, and 100 mm indicated that they felt exactly as if their own finger was moving. Data analysis. Descriptive statistics, including the mean and standard deviation (S.D.), were calculated for all variables. A one-way analysis of variance (ANOVA) was used to assess the effect on the MEP amplitude of the “condition” factor [Resting (Group A and Group B, n⫽20), Illusion (Group A and Group B,
F. Kaneko et al. / Neuroscience 149 (2007) 976 –984 n⫽20), Non-illusion (Group A, n⫽10), and Sham (Group B, n⫽10)] as shown for each coil individually (RdA or RdB). The Tukey-Kramer method was used as a post hoc test after one-way ANOVA to test whether the MEP amplitudes were significantly modulated according to conditions for each coil. The increase ratio (MEP amplitude in the index-abd condition/MEP amplitude at rest) was calculated as the variable indicating the strength of the MEP’s facilitation induced by the illusory visual stimuli of the movie of the index finger movement, both for the first dorsal interosseous and for the abductor digiti minimi. Differences in this increase ratio between first dorsal interosseous and abductor digiti minimi, MEP latency at rest condition between RdA and RdB, and resting motor threshold between RdA and RdB were statistically analyzed using paired t-test.
Experiment 2 Subjects. Six neurologically healthy male subjects (age 21–31 years) participated in experiment 2. All subjects were selfdeclared right-hand dominant. Each gave his informed consent for the experiment. Four subjects had participated in experiment 1, and another two subjects participated only in this experiment. Procedures. EMG recording and TMS were carried out in almost same manner as that of experiment 1. The difference between experiment 1 and 2 was that TMS stimuli were delivered only with RdB since the effect of the illusion condition in experiment 1 was more obviously shown in the MEP results using RdB. As in experiment 1, the resting condition was the first round in experiment 2. Other experimental conditions included index-abd (“illusion” in experiment 1), index-add, little-abd, and little-add, for a total of five conditions including resting. MEP responses were elicited while the subject watched the movie on the computer screen set on his forearm precisely to induce the illusory feeling as if own finger were actually moving. In this movie, someone else’s index finger or little finger was abducted (index-abd, little-abd) (Fig. 1E) or adducted (index-add, little-add). In all the cases TMS was delivered at the middle range of the movement (abduction or adduction) of the fingers in the movie. The index-add, little-abd, and little-add conditions were control conditions against the index-abd to discover whether MEP facilitation of the first dorsal interosseous induced during the illusion condition in experiment 1 (“index-abd” in experiment 2) was limited to the index finger and to abduction as opposed to adduction. During these trials, the subject’s index and little finger were statically held in mid-position aligned with the 2nd and 5th metacarpal bone, respectively, as in experiment 1. VAS was used to evaluate the introspective response in each subject during the index-abd and little-abd conditions, as in experiment 1. Data analysis. A one-way ANOVA with repeated measures was used to assess the effect on the MEP amplitude of “condition” factors (resting, index-abd, index-add, little-abd, little-add). The difference in MEP between each pair of conditions was examined using the Tukey-Kramer method. This statistical analysis determined whether MEP facilitation depended on the movement direction and the part of the body being moved. Differences of the strength of the illusory feeling (VAS value of introspection) between the index and little finger versions of the movie were statistically analyzed using paired t-test. Spearman’s correlation coefficient by rank between the values of VAS during illusion condition of index finger movement (independent variable) and the increase ratios of MEP recorded from the first dorsal interosseous (dependent variable) was calculated under the linear regression methods.
RESULTS Experiment 1 Superimposed MEP specimen records induced using RdB are shown in Fig. 2. Under the illusion condition, selective
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enlargement of the MEP amplitude recorded from first dorsal interosseous can be seen. No similar enlargement was observed in the MEP recorded from the abductor digiti minimi. Fig. 3 shows the average (⫾S.D.) MEP recorded from the first dorsal interosseous (Fig. 3A) and abductor digiti minimi (Fig. 3B) in each condition. There were significant differences in MEP amplitudes between the conditions for the first dorsal interosseous regardless of the coil orientation (RdA: F3,56⫽4.65, P⬍0.01; RdB: F3,56⫽6.94, P⬍0.001) (Fig. 3A). The post hoc test revealed that MEP amplitudes recorded from the first dorsal interosseous under the illusion condition were significantly larger than those induced under the other two RdA conditions and also under the other three RdB conditions. On the other hand, there was no significant difference in MEP amplitudes among the conditions for the abductor digiti minimi (RdA: F3,56⫽1.19, P⫽0.32; RdB: F3,56⫽1.17, P⫽0.33) (Fig. 3B). MEP facilitation produced by the illusory visual stimulus of the index finger abduction was detected selectively in the first dorsal interosseous. MEP latency in the first dorsal interosseous and also in the abductor digiti minimi induced by means of RdA at rest (the first dorsal interosseous: 24.30⫾1.68 ms; the abductor digiti minimi: 24.29⫾1.62 ms) was significantly slower than that induced using RdB (the first dorsal interosseous: 23.17⫾1.49 ms; the abductor digiti minimi: 23.32⫾1.71 ms) (the first dorsal interosseous: t(19)⫽9.05, P⬍0.0001; the abductor digiti minimi: t(19)⫽4.89, P⫽0.001). The resting motor threshold of RdA (70.75⫾12.68%) was significantly higher than that of RdB (55.35⫾10.99%) (t(19)⫽11.36, P⬍0.0001). A paired t-test was used to evaluate the difference in the MEP increase ratio between the first dorsal interosseous and abductor digiti minimi, which suggests the strength of the MEP facilitation induced by the illusion condition compared with that induced in the resting condition. The increase ratio of the MEP induced from the first dorsal interosseous (1.97⫾1.10) was significantly larger than that from the abductor digiti minimi (1.42⫾0.87) (t(19)⫽2.41, P⫽0.026). In post-experiment interviews, the subjects commented as follows: In the illusion condition, they felt strongly as if their own finger was actually moving. In the non-illusion condition, however, they clearly recognized that their own finger was relaxed while someone else’s finger was abducting on the screen. More or less, all of the subjects answered that they felt as if their own hand was passively moving in the illusion condition. The average response on VAS for this condition was 55.2⫾ 17.4 mm. Experiment 2 MEP amplitudes recorded from the first dorsal interosseous and abductor digiti minimi in each condition are presented in Fig. 4. There was a significant main effect for the “condition” factor (F3,5⫽3.95, P⫽0.029) among the five conditions for MEP recorded from the first dorsal interosseous. On the other hand, MEP amplitudes recorded from the abductor digiti minimi showed no significant effect for the “condition” factor (F3,5⫽2.59, P⫽0.091). In the post hoc test, the MEP
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Fig. 2. Superimposed MEP specimen records induced using RdB during the four conditions from one subject each belonging to group A (A) and group B (B) in experiment 1.
amplitude recorded from the first dorsal interosseous during index-abd was significantly larger than those during all another conditions (P⬍0.05). Though MEP amplitude in the first dorsal interosseous induced in the index-abd condition was significantly facilitated compared with that in the resting condition, there was no significant facilitation of MEP response in the other three control conditions (indexadd, little-abd, little-add). The results of VAS interviews to evaluate introspective responses showed that a significantly strong illusory feeling was induced during movement of the index finger compared with the movement of the little finger (VAS of the index finger movement, 76.7⫾12.2 mm; VAS of the little finger movement, 52.8⫾23.4 mm; t(5)⫽4.11; P⫽0.009). There was no definitive correlation between VAS and increase ratio on MEP (Rho⫽⫺0.36, P⫽0.425).
DISCUSSION The most important point in the present study was whether there was a significant difference in MEP facilitation between the conditions of illusion and non-illusion in experiment 1. The essential difference that those two conditions
represent is the presence or absence of an introspective kinesthetic illusion during task execution, though both the illusion and non-illusion conditions have the element of observing biological action. According to the results of VAS interviews in experiments 1 and 2, the illusory visual stimulus gave subjects the distinct impression that their own fingers were actually moving even though the subjects’ hands were actually stationary. The present results in experiment 1 showed significant facilitation of MEP under the illusion condition compared with that under the non-illusion condition, which was conducted as a control condition. On the other hand, MEP during non-illusion was not significantly facilitated compared with that during the resting and sham conditions, although the average value during the non-illusion was generally higher than that during the resting and sham conditions. This absence of significance does not contradict the previous studies showing that simply observing action facilitated MEP (Fadiga et al., 1995; Gangitano et al., 2004; Maeda et al., 2001, 2002; Strafella and Paus, 2000). Based on the experience-dependent modulation of corticospinal excitability during action observation (Maeda et al., 2001, 2002), the moving hand orien-
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Fig. 3. Average⫾S.D. of MEPs recorded from the first dorsal interosseous (A) and abductor digiti minimi (B) during the four conditions of experiment 1. MEP elicited in the illusion condition was significantly greater than that in the resting and sham conditions for both RdA and RdB, and also greater than that in the non-illusion condition for RdB. (* Indicates the Tukey-Kramer test with a significant level of P⬍0.05.)
tation in this experiment might be not sufficient to facilitate MEP in a non-illusion condition. While facilitation of MEP in an observer by someone else’s hand oriented in a position directed toward the subject’s body has been reported (Maeda et al., 2001, 2002), the hand orientation during the non-illusion condition in this study was directed away from the subject’s body. We speculate that the inappropriate hand orientation in the non-illusion condition may have caused the absence of marked MEP facilitation during the non-illusion condition although the hand orientation adopted for the non-illusion condition corresponded with that used during the illusion condition. Montagna et al. (2005) reported that motor excitability was changed during the observation of a meaningful hand movement executed by someone else, but the orientation of the observed hand in our movie did not correspond to the experience of the observer in their experiment. That the finger movement in the movie of our study was meaningless may be one of the reasons why the non-illusion condition did not facilitate
MEP amplitude. Furthermore, the fact that the subjects could see their actual static hand below the movie might be the most important reason. The previous research have reported that the cortical motor areas are activated during kinesthetic illusory feeling induced by tendon vibration (Naito et al., 1999, 2002, 2005, 2006; Romaiguere et al., 2003, 2005; Naito, 2004; Naito and Ehrsson, 2001, 2006; Casini et al., 2006). In opposition to the kinesthetic illusion effect of the tendon vibration, we clarified that the kinesthetic illusory feeling carried from our experimental visual input induces a facilitatory effect on corticomotor pathways including cortical motor areas, although there was no mechanical input to the muscle spindle. Activation of the abductor digiti minimi, which is the synergistic muscle of the first dorsal interosseous that opens the hand, was not significantly affected by observation of movement by the index finger or little finger. The results of a direct comparison of MEP facilitation (the increase ratio) between the first dorsal interosseous and
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Fig. 4. Average⫾S.D. of MEPs recorded from the first dorsal interosseous and abductor digiti minimi during the five conditions of experiment 2. In index-abd (the “illusion” condition in experiment 1), the MEP recorded from the first dorsal interosseous was significantly greater than those in all another conditions. There was no statistical significance of the MEP amplitude from the abductor digiti minimi.
abductor digiti minimi showed that the extent of facilitation of MEP was obviously greater in the first dorsal interosseous than that in the abductor digiti minimi. This result indicates that, as expected, the effect of the illusion was stronger to the same muscle in the observer as that observed moving on the screen than the synergistic muscle. However, MEP facilitation during the illusory condition does not seem to be common for all body parts. The results of experiment 2, in which MEP facilitation was shown only in the first dorsal interosseous during indexabd, while little-abd did not affect the facilitation to the abductor digiti minimi, support the body-part dependence of the effect of the illusory condition. This contradiction of the effects of the illusory condition on MEP facilitation between the movements by the index finger and little finger may be caused by the strength of the visuomotor relationship or visual experience, since the frequency of seeing index finger movement in daily living is surely higher than that of little finger movement. This point is a prospective research subject. The finding of the present research is that the kinesthetic illusory feeling induced by a visual stimulus and MEP facilitation was stronger in the case of the index finger than in that of the little finger. In experiment 2, MEP induced in the first dorsal interosseous during the illusory condition did not change in the index-add condition. This result indicates that the effect of the illusory condition on corticomotor excitability, which corresponds to the cortical portion that drives the first dorsal interosseous, is dependent on the movement direction. In this point, a function of the mirror neuron network was reported as the presence of a strict temporal coupling between the corticospinal excitability and the dynamics of movements has been reported (Gangitano et al., 2001; Nishitani and Hari, 2000; Oouchida et al., 2004; Terao and Ugawa, 2002), though a relevancy to the present results was unknown.
The moving text observation in this experiment (sham condition) did not induce any significant effects in either the first dorsal interosseous or abductor digiti minimi. This result may support the suggestion that the facilitative visual input on a screen must be an action executed by a human figure (Tai et al., 2004). Introducing kinematic laws of biological movement into the movie may have facilitated the illusion. On the other hand, the facilitatory effect of the illusory condition on corticomotor pathways indicates that even an intransitive meaningless movement in humans can activate the motor output system, whereas such a movement does not activate mirror neurons in monkeys (Rizzolatti, 2005; Rizzolatti and Craighero, 2004). The dominance of vision with respect to body image recognition associated with somatosensory information was confirmed by Botvinick and Cohen (1998), although their experimental condition was only a resting one. They reported that the subjects experienced an illusion of tactile perception in which they felt touch at the locus of a rubber arm. This rubber-arm illusion reveals that a three-way interaction between vision, touch and proprioception creates the illusion of tactile perception. According to other authors who replicated their experiment, the displacement of tactile sensations and the illusion of ownership disappear if the rubber arm is not properly aligned with the subject’s body (van den Bos and Jeannerod, 2002). In the present study’s illusion condition, accurate manipulation of the alignment between actual body and displayed body was a key condition for making the subjects feel the kinesthetic illusion from the visual input. Furthermore, kinematic information from an observed movie seemed to be a key point for observers to distinguish whether the performer in the movie is one’s self or someone else (Daprati et al., 2007). Because the index and little fingers in our movie were passively moved by our experimental device at
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constant angular velocity (isokinetic), there was no individual kinematic property to those movements in the movie. The absence of the properties of active finger movement in the movie may have helped induce the illusory feeling by allowing the subject to forget that he was not the owner of the fingers in the movie. The illusion condition in the present study was novel. The visual stimulus, which was carried in the study of Tardy-Gervet et al. (1982, 1984) was that the background figure shown under the subject’s hand was moved when the subject was seeing his own hand and ambient circumstances through a pinhole. The conditions of Ramachandran et al. (1995, 1996) and Giraux and Sirigu (2003) seem markedly similar to the illusion condition in this study, but the amputee patients also observed their own hand movements. The point of contrast with our research is that the subjects in these prior studies actually observed their own hands. Furthermore, there was voluntary movement on opposite sides in the Ramachandran et al. report. That the manner of the present visual stimulus could induce MEP enhancement suggests that an introspective kinesthetic illusion can be induced under a visual condition, without voluntary motor output from the opposite side or an actual picture of one’s own hand. In terms of clinical relevance, the present approach may offer the possibility of having applications for neuro-rehabilitation since this approach can be interpreted as “passive visual motor imagery.” It is known that an electrical current delivered by means of a circular coil positioned flat at the vertex can activate the motor cortex preferentially when the induced current flows from back to front, or non-preferentially when the current in the brain flows from front to back (Trompetto et al., 1999). In RdA, the coil current flows counterclockwise, so that the current induced in the brain flows clockwise. On the contrary, when the RdB is placed on the skull, the current induced in the brain is counterclockwise. TMS in this case induces MEP preferentially to record from a muscle in the left side. Different neural circuits having different motor thresholds and MEP latencies are recruited depending on which side of the coil faces up (Day et al., 1989; Wilson et al., 1996; Trompetto et al., 1999; Terao and Ugawa, 2002). The present results showed that MEP latency induced at rest by means of RdA was significantly longer than that induced by RdB and that the resting motor threshold induced by RdA was significantly higher than that induced by RdB. The absence of MEP amplitude differences between MEPs induced by RdA and RdB as shown in the present results suggests that the facilitatory effect carried over from a visual input affected both neuronal chains.
CONCLUSION In conclusion, a new finding in the present study is that, first, the kinesthetic self-movement illusion can be induced by our experimental condition in which a video of a moving finger was shown with the display situated so that the video hand overlaps closely with the subject’s actual hand. Second, the illusion condition causes a measurable physiolog-
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ical effect (facilitatory effect of input to corticomotor pathways), though the facilitatory effect was shown only when the index finger was abducting in the video from the agonist muscle first dorsal interosseous. These findings mean the kinesthetic illusion is not just a process of movement recognition but also has a functional role of modulating excitability in corticomotor pathways. We think that there is a value to ascertaining whether our experimental method using video is as effective as the rehabilitation intervention to facilitate recovery of motor function, for example in a stroke patient.
REFERENCES Borroni P, Montagna M, Cerri G, Baldissera F (2005) Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement. Brain Res 1065:115–124. Botvinick M, Cohen J (1998) Rubber hands “feel” touch that eyes see. Nature 391:756. Calvin-Figuiere S, Romaiguere P, Gilhodes JC, Roll JP (1999) Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration. Exp Brain Res 124:342–350. Calvin-Figuiere S, Romaiguere P, Roll JP (2000) Relations between the directions of vibration-induced kinesthetic illusions and the pattern of activation of antagonist muscles. Brain Res 881:128–138. Casini L, Romaiguere P, Ducorps A, Schwartz D, Anton JL, Roll JP (2006) Cortical correlates of illusory hand movement perception in humans: a MEG study. Brain Res 1121:200 –206. Daprati E, Wriessnegger S, Lacquaniti F (2007) Kinematic cues and recognition of self-generated actions. Exp Brain Res 177:31– 44. Day BL, Dressler D, Maertens de Noordhout A, Marsden CD, Nakashima K, Rothwell JC, Thompson PD (1989) Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol 412:449 – 473. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608 –2611. Gangitano M, Mottaghy FM, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. Neuroreport 12:1489 –1492. Gangitano M, Mottaghy FM, Pascual-Leone A (2004) Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci 20:2193–2202. Giraux P, Sirigu A (2003) Illusory movements of the paralyzed limb restore motor cortex activity. Neuroimage 20 (Suppl 1):S107–S111. Jeannerod M (2003) The mechanism of self-recognition in humans. Behav Brain Res 142:1–15. Maeda F, Chang VY, Mazziotta J, Iacoboni M (2001) Experiencedependent modulation of motor corticospinal excitability during action observation. Exp Brain Res 140:241–244. Maeda F, Kleiner-Fisman G, Pascual-Leone A (2002) Motor facilitation while observing hand actions: specificity of the effect and role of observer’s orientation. J Neurophysiol 87:1329 –1335. Montagna M, Cerri G, Borroni P, Baldissera F (2005) Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action. Eur J Neurosci 22:1513–1520. Naito E (2004) Sensing limb movements in the motor cortex: how humans sense limb movement. Neuroscientist 10:73– 82. Naito E, Ehrsson HH (2001) Kinesthetic illusion of wrist movement activates motor-related areas. Neuroreport 12:3805–3809. Naito E, Ehrsson HH (2006) Somatic sensation of hand-object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci 26:3783–3790. Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a positron emission tomography study. J Neurosci 19:6134 – 6144.
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Naito E, Roland PE, Ehrsson HH (2002) I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement. Neuron 36:979 –988. Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, Zilles K, Ehrsson HH (2005) Dominance of the right hemisphere and role of area 2 in human kinesthesia. J Neurophysiol 93:1020 –1034. Nishitani N, Hari R (2000) Temporal dynamics of cortical representation for action. Proc Natl Acad Sci U S A 97:913–918. Oouchida Y, Okada T, Nakashima T, Matsumura M, Sadato N, Naito E (2004) Your hand movements in my somatosensory cortex: a visuo-kinesthetic function in human area 2. Neuroreport 15:2019 –2023. Ramachandran VS, Rogers-Ramachandran D (1996) Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci 263:377–386. Ramachandran VS, Rogers-Ramachandran D, Cobb S (1995) Touching the phantom limb. Nature 377:489 – 490. Rizzolatti G (2005) The mirror neuron system and its function in humans. Anat Embryol (Berl) 210:419 – 421. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169 –192. Romaiguere P, Anton JL, Roth M, Casini L, Roll JP (2003) Motor and parietal cortical areas both underlie kinaesthesia. Cogn Brain Res 16:74 – 82. Romaiguere P, Calvin S, Roll JP (2005) Transcranial magnetic stimulation of the sensorimotor cortex alters kinaesthesia. Neuroreport 16:693– 697. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH, et al. (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79 –92.
Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W (1999) Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52:97–103. Scott J, Huskisson EC (1976) Graphic representation of pain. Pain 2:175–184. Strafella AP, Paus T (2000) Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11:2289 –2292. Tai YF, Scherfler C, Brooks DJ, Sawamoto N, Castiello U (2004) The human premotor cortex is “mirror” only for biological actions. Curr Biol 14:117–120. Tardy-Gervet MF, Gilhodes JC, Roll JP (1982) Demonstration of an illusory limb movement and associated motor activities induced by a moving visual stimulus in man. A descriptive study. Neurosci Lett 28:187–192. Tardy-Gervet MF, Gilhodes JC, Roll JP (1984) Perceptual and motor effects elicited by a moving visual stimulus below the forearm: an example of segmentary vection. Behav Brain Res 11:171–184. Terao Y, Ugawa Y (2002) Basic mechanisms of TMS. J Clin Neurophysiol 19:322–343. Trompetto C, Assini A, Buccolieri A, Marchese R, Abbruzzese G (1999) Intracortical inhibition after paired transcranial magnetic stimulation depends on the current flow direction. Clin Neurophysiol 110:1106 –1110. van den Bos E, Jeannerod M (2002) Sense of body and sense of action both contribute to self-recognition. Cognition 85:177–187. Wilson SA, Day BL, Thickbroom GW, Mastaglia FL (1996) Spatial differences in the sites of direct and indirect activation of corticospinal neurones by magnetic stimulation. Electroencephalogr Clin Neurophysiol 101:255–261.
(Accepted 21 July 2007) (Available online 1 August 2007)
KINESTHETIC ILLUSORY FEELING INDUCED BY A FINGER MOVEMENT MOVIE EFFECTS ON CORTICOMOTOR EXCITABILITY F. KANEKO,a* T. YASOJIMAa AND T. KIZUKAb
our visual stimulus method in the present study. The method of visual stimulus presentation was a movie in which someone else’s limb (an index finger in the present study) is moving. The computer screen on which the movie played was installed on an appropriate portion of the subject’s forearm, so that the performer’s hand appears as if it were the subject’s hand. The objective of our study was to clarify whether an illusion originating from visual input affects cortical level excitability: that is to say, whether a “sensory” illusion induced by this novel approach has a measurable “motor” effect. Since perceptual-to-motor transformation during tendon vibration was demonstrated by motor unit activity recording from an antagonist muscle of the vibrated muscle (Calvin-Figuiere et al., 1999, 2000; Romaiguere et al., 2005), if a similar effect were to be found in our experimental visual stimulus, it may be useful to provide a facilitatory effect to the corticomotor pathways corresponding to rehabilitation of patients with motor disorders of some kind. Many experimental results stress a prevalent role of vision over other senses in self-recognition, though it is largely context-dependent: we feel our hand where we see it, not the converse (Jeannerod, 2003). Various studies have concurred upon an understanding of the dominance of visual afferent information with respect to awareness of somatosensory information, and also that such information influences corticomotor excitability. The induction of a kinesthetic illusory sensation by moving visual stimulus of ambient circumstances surrounding a subject’s static hand was reported by Tardy-Gervet et al. (1982, 1984). Furthermore, it was shown that a kinesthetic illusion could be induced in arm-amputees by their observing a motion executed by the opposite, intact hand in a mirror. Ramachandran and Rogers-Ramachandran (1996) reported that most of the amputees who participated in the experiment felt an emerging, vivid kinesthetic sensation of the phantom movement in the mirror. The condition in the present study by which a movie is presented, is based on another kind of knowledge, that is, the evidence about the dominance of vision with respect to body image recognition that is associated with having somatosensory information (Botvinick et al., 1998; van den Bos and Jeannerod, 2002). The necessary condition is for there to be a precise alignment between the subject’s actual body and the performer’s body in the display. The condition settings adopted in the present study are basically different from those used in previous studies. The body observed by the subject is that of someone else; there is no voluntary action on the contralateral side during the observation; the observed person’s hand faces away from the subject, and the observed
a
Institute for Human Science and Biomedical Engineering, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba City, Ibaraki 305-8566, Japan
b
Graduate School of Comprehensive Human Sciences, University of Tsukuba, 1-1-1 Tennoudai, Tsukuba City, Ibaraki 305-8574, Japan
Abstract—The present study aimed to clarify whether a kinesthetic illusion arises in our experimental condition (visual stimulus) and whether corticomotor excitability changes in parallel with the kinesthetic illusion. The visual stimulus was a movie in which someone else’s limb was being moved. The computer screen showing the movie was installed at an appropriate portion of the subject’s forearm, so that the performer’s hand appeared as if it were the subject’s hand (illusion). The experience of kinesthetic illusion under this condition was verified by interview using a visual analog scale. Healthy male subjects participated in this experiment. Transcranial magnetic stimulation was applied to induce motorevoked potential (MEP) from the first dorsal interosseous and abductor digiti minimi muscle. Each subject was instructed to watch the same computer display shown as in the illusion, with his own stationary hand in full view (non-illusion) and to watch a display of non-biological movement (moving text) (sham) as the control conditions. The present results showed significant facilitation of MEP under the illusion compared with the control conditions for the index finger abducting in the movie, although not for adducting. MEP in the abductor digiti minimi showed no change during either abduction or adduction of the little finger. The present study demonstrated that an illusion of self-motion can be created by a video of a moving abstract index finger, and inputs to the corticomotor pathways during the self-motion illusion facilitated the corticomotor excitability. The excitatory effect of the illusion depended on the movement direction of the index finger. © 2007 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: kinesthesia, illusion, transcranial magnetic stimulation, motor-evoked potential, mirror neuron system.
It has been found that kinesthetic illusions of limb movement induced by tendon vibration against the muscle spindle alter sensorimotor cortex excitability with the reception of sensory afferent input, despite the fact that the vibrated limb remains immobile (Naito et al., 1999, 2002, 2005, 2006; Calvin-Figuiere et al., 1999, 2000; Romaiguere et al., 2003, 2005; Naito, 2004; Naito and Ehrsson, 2001, 2006; Casini et al., 2006). We investigate whether a kinesthetic illusory sensation could be induced in a subject by *Corresponding author. Tel: ⫹81-29-861-7885; fax: ⫹81-29-861-6660. E-mail address: [email protected] (F. Kaneko). Abbreviations: ANOVA, analysis of variance; EMG, electromyography; MEP, motor-evoked potential; TMS, transcranial magnetic stimulation; VAS, visual analog scale.
0306-4522/07$30.00⫹0.00 © 2007 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2007.07.028
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object is a computer display (not a mirror or an actual body). First, the aim of the present study was to clarify whether the kinesthetic illusion arises in our experimental condition. Second, we tested an input originating from the self-movement illusion affecting the corticomotor excitability in parallel with the kinesthetic illusion during that condition.
EXPERIMENTAL PROCEDURES Experiment 1 Subjects. Twenty neurologically healthy male subjects (age 21–31 years) participated in this experiment. All subjects were self-declared right-hand dominant. Each gave his informed consent for the experiment, which was approved by the local ethics committee. The subjects were divided into Group A and Group B. Ten subjects (Group A) underwent the resting, illusion, and nonillusion conditions, and the other 10 subjects (Group B) underwent the resting, illusion, and sham conditions. The groups were divided this way because the number of transcranial magnetic stimulations (TMS) subjects might undergo would be over the limit established by the local ethics committee if all four conditions were employed on each subject. Electromyography (EMG) recording and TMS. Surface EMG signals were recorded from the first dorsal interosseous muscle and from the abductor digiti minimi muscle of the left side using bipolar surface electrodes. The Ag–AgCl disc electrodes (5 mm in diameter) were arranged at 10 mm intervals. Before the electrodes were attached, the skin area was rubbed with alcohol and abraded with abrasive skin-prepping gel. EMG signals were amplified (Neuropack MEB-2200, Nihonkoden Co. Ltd., Toyko, Japan) at an appropriate level (⫻1000) and filtered (5.3–1000 Hz). The EMG signal, a trigger signal to be carried to the transcranial magnetic stimulator (Magstim 200, The Magstim Co. Ltd., Wales, UK), and the output signal of the stimulation from the Magstim 200 were digitized at 20 kHz per channel by a CED 1401 (Cambridge Electronic Design Limited, Cambridge, UK) using a personal computer. A round coil with a 9-cm outside diameter was used to elicit motor-evoked potential (MEP) both from the single target muscle, which is the agonist muscle of the index finger movement, and from a control muscle (the abductor digiti minimi) close to the first dorsal interosseous. For each condition TMS was applied to induce MEP and was delivered through a round coil placed so that the A or B side faced up (RdA or RdB) around Cz. MEP was obtained in accordance with a report of the International Federation of Clinical Neurophysiology (Rossini et al., 1994; Rothwell et al., 1999). TMS was applied during the resting condition before the other three conditions. MEP was recorded from the first dorsal interosseous and abductor digiti minimi. The resting motor thresholds were defined as the minimal intensity capable of inducing MEP with a peak-to-peak amplitude greater than 50 V in both coils in at least four out of seven trials. During testing, the TMS stimulus intensity capable of inducing MEP with peak-to-peak average amplitudes of 0.5–1 mV during the resting condition was also used in the other three conditions. As a result, TMS was delivered at 114.61⫾7.91% (mean⫾S.D.) of the subjects’ resting motor threshold in all trials. MEPs were induced at least 10 times for each condition. The EMGs, which were shown on a computer display (17 inches), were monitored by more than two experimenters in all of the stimulations with a 500 V scale per division (a total of 10 divisions for each muscle); the experimenters were required to reject the trial if tiny muscle activation was recognized during testing. Furthermore, the absence of EMG activation during each test was visually reconfirmed offline after the experiments.
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Supramaximal M-waves were recorded by applying an electrical current to the ulnar nerve from both the first dorsal interosseous and abductor digiti minimi after TMS testing. The current intensity was gradually increased, and the peak amplitude of the M-wave was visually confirmed. The amplitudes from the MEP of both the first dorsal interosseous and abductor digiti minimi were normalized individually with the supramaximal M-wave amplitude. Procedures. During the experiment, the subject sat in a comfortable chair with his left hand on a custom-built experimental table. Comfortable positions for the joints were established depending on each subject in such a way that the shoulder joint was set at almost 45° abduction and flexion, and the elbow joint was positioned at about 30° flexion. The condition of the first experimental block was the resting condition, in which the TMS was applied before then being applied to the other conditions in random order. The order for RdA vs. RdB was randomized for the subjects. Two kinds of control conditions (“non-illusion” and “sham”) against the illusion condition were adopted to compare the illusory effect on corticomotor pathways. In the next experimental block, the resting condition was followed randomly by either RdA and RdB in the following three conditions. In the illusion condition, a computer screen showing the abduction of someone else’s index finger was placed on the subject’s left side distal forearm. The position of the screen was adjusted so that the subject would see the action on the screen as if watching his own index finger moving (Fig. 1A). While the screen was being pre-set, the subject was interviewed to confirm whether the adjustment of its position was appropriate to induce a kinesthetic illusion. Fig. 1B illustrates how the performer’s index finger was passively moved by our experimental device in the movie presented on the screen. In the non-illusion condition, the subject was instructed to watch the same computer screen showing the abduction of someone else’s index finger, only the subject could recognize that his own finger was not moving since his own static hand was in his field of view (Fig. 1C). In the sham condition, the subject was shown white 3D text (“Microsoft Windows”) on the black computer screen, running from left to right with rotating in the side direction. This was the screen saver function of Microsoft Windows XP. This particular text was chosen as being unlikely to induce imagery relating to body movement. Visual stimulus of someone else’s hand action. In this study, a specialized visual feedback condition was formulated for future clinical applications of kinesthetic illusion. The movie had been made prior to the experiment. The performer, who did not participate in the TMS experiment, sat in a comfortable chair with his left hand on a custom-built experimental table in the same manner as in the TMS experiment while the movie was made. This performer’s body physique and skin color were easily recognizable as those of an average Japanese man. A consumer-type digital video camera (HDR-HC1, Sony Style (Japan) Inc., Tokyo, Japan) was carefully positioned beside the performer’s face at eye level so that the camera angle would be the same as the angle of the eyes in regard to the index finger movement. The angle between performer’s index finger and thumb was set at 80° in their initial positions. The movement axis of the index finger’s abduction/adduction was positioned on the servomotor’s axis built in to the device (Fig. 1B). The motion of the digit saucer, in which index finger was placed, was controlled by personal computer. At the start of the movie, the index finger was adducted and in contact with the middle finger. The passive abduction took 3 s, and the 3-s adduction of the index finger made an entire “round” lasting 6 s. In both the illusion and non-illusion conditions, the computer screen on which the movie played was installed on an appropriate portion of the subject’s forearm. The movie (QuickTime ver. 7.1.3, Apple Computer, Inc., CA, USA) window in the display was adapted to the subject’s body size by changing the window size so that the presentation of the performer’s hand could be adjusted to the
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Fig. 1. Three conditions in experiment 1 (A–D) and an additional condition performed in experiment 2 (E) are shown. Illusion: A computer screen showing the abduction of someone else’s index finger was placed on the subject’s distal forearm. The position of the screen was adjusted accurately so that the subject would see the action on the screen as if watching his own index finger moving (Fig. 1A). Fig. 1B illustrates the hand setting and index finger movement in the movie. The index finger was passively moved by an experimental device; one “round” of abduction and adduction took a total of 6 s. Non-illusion: Subject was instructed to watch a computer screen showing the abduction of someone else’s index finger, as in the illusion condition. The difference between the illusion and non-illusion conditions was that, in the latter condition, the subject could recognize that his own finger was not moving because his own static hand remained in his field of view (Fig. 1C). Sham: Subject was shown white 3D text moving on the black background of the computer screen, which was set up in the same position as in the illusion condition (Fig. 1D). In experiment 2, a movie of the little finger being moved (abduction and adduction) was added as a control condition. The little finger of the left hand was set on the digit saucer in the conditions little-abd and little-add.
subject’s hand size. TMS was applied at the point when the index finger in the movie was in the middle position of its abduction movement range once every two or three rounds. This stimulus timing was one of the important points, since it was elucidated that the motor excitability during the observation of a certain action changes depending on a cyclic time course (Borroni et al., 2005; Montagna et al., 2005). For the illusion and non-illusion conditions, the subject’s actual index finger was statically held on the experimental table in a 30° degree abduction position to the middle finger and the subject was directed to rest it there throughout the testing conditions. Evaluation of introspection. A visual analog scale (VAS) was adopted to evaluate the introspective perception in the
illusion condition (Scott and Huskisson, 1976). Subjects were interviewed concerning how strongly they experienced the introspective perception associated with the kinesthetic sense of their own finger movement after the illusion condition session, so that their answer includes strength of the feeling about movement and ownership. In the present study, zero indicated that the subjects had no illusory sensation at all, and 100 mm indicated that they felt exactly as if their own finger was moving. Data analysis. Descriptive statistics, including the mean and standard deviation (S.D.), were calculated for all variables. A one-way analysis of variance (ANOVA) was used to assess the effect on the MEP amplitude of the “condition” factor [Resting (Group A and Group B, n⫽20), Illusion (Group A and Group B,
F. Kaneko et al. / Neuroscience 149 (2007) 976 –984 n⫽20), Non-illusion (Group A, n⫽10), and Sham (Group B, n⫽10)] as shown for each coil individually (RdA or RdB). The Tukey-Kramer method was used as a post hoc test after one-way ANOVA to test whether the MEP amplitudes were significantly modulated according to conditions for each coil. The increase ratio (MEP amplitude in the index-abd condition/MEP amplitude at rest) was calculated as the variable indicating the strength of the MEP’s facilitation induced by the illusory visual stimuli of the movie of the index finger movement, both for the first dorsal interosseous and for the abductor digiti minimi. Differences in this increase ratio between first dorsal interosseous and abductor digiti minimi, MEP latency at rest condition between RdA and RdB, and resting motor threshold between RdA and RdB were statistically analyzed using paired t-test.
Experiment 2 Subjects. Six neurologically healthy male subjects (age 21–31 years) participated in experiment 2. All subjects were selfdeclared right-hand dominant. Each gave his informed consent for the experiment. Four subjects had participated in experiment 1, and another two subjects participated only in this experiment. Procedures. EMG recording and TMS were carried out in almost same manner as that of experiment 1. The difference between experiment 1 and 2 was that TMS stimuli were delivered only with RdB since the effect of the illusion condition in experiment 1 was more obviously shown in the MEP results using RdB. As in experiment 1, the resting condition was the first round in experiment 2. Other experimental conditions included index-abd (“illusion” in experiment 1), index-add, little-abd, and little-add, for a total of five conditions including resting. MEP responses were elicited while the subject watched the movie on the computer screen set on his forearm precisely to induce the illusory feeling as if own finger were actually moving. In this movie, someone else’s index finger or little finger was abducted (index-abd, little-abd) (Fig. 1E) or adducted (index-add, little-add). In all the cases TMS was delivered at the middle range of the movement (abduction or adduction) of the fingers in the movie. The index-add, little-abd, and little-add conditions were control conditions against the index-abd to discover whether MEP facilitation of the first dorsal interosseous induced during the illusion condition in experiment 1 (“index-abd” in experiment 2) was limited to the index finger and to abduction as opposed to adduction. During these trials, the subject’s index and little finger were statically held in mid-position aligned with the 2nd and 5th metacarpal bone, respectively, as in experiment 1. VAS was used to evaluate the introspective response in each subject during the index-abd and little-abd conditions, as in experiment 1. Data analysis. A one-way ANOVA with repeated measures was used to assess the effect on the MEP amplitude of “condition” factors (resting, index-abd, index-add, little-abd, little-add). The difference in MEP between each pair of conditions was examined using the Tukey-Kramer method. This statistical analysis determined whether MEP facilitation depended on the movement direction and the part of the body being moved. Differences of the strength of the illusory feeling (VAS value of introspection) between the index and little finger versions of the movie were statistically analyzed using paired t-test. Spearman’s correlation coefficient by rank between the values of VAS during illusion condition of index finger movement (independent variable) and the increase ratios of MEP recorded from the first dorsal interosseous (dependent variable) was calculated under the linear regression methods.
RESULTS Experiment 1 Superimposed MEP specimen records induced using RdB are shown in Fig. 2. Under the illusion condition, selective
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enlargement of the MEP amplitude recorded from first dorsal interosseous can be seen. No similar enlargement was observed in the MEP recorded from the abductor digiti minimi. Fig. 3 shows the average (⫾S.D.) MEP recorded from the first dorsal interosseous (Fig. 3A) and abductor digiti minimi (Fig. 3B) in each condition. There were significant differences in MEP amplitudes between the conditions for the first dorsal interosseous regardless of the coil orientation (RdA: F3,56⫽4.65, P⬍0.01; RdB: F3,56⫽6.94, P⬍0.001) (Fig. 3A). The post hoc test revealed that MEP amplitudes recorded from the first dorsal interosseous under the illusion condition were significantly larger than those induced under the other two RdA conditions and also under the other three RdB conditions. On the other hand, there was no significant difference in MEP amplitudes among the conditions for the abductor digiti minimi (RdA: F3,56⫽1.19, P⫽0.32; RdB: F3,56⫽1.17, P⫽0.33) (Fig. 3B). MEP facilitation produced by the illusory visual stimulus of the index finger abduction was detected selectively in the first dorsal interosseous. MEP latency in the first dorsal interosseous and also in the abductor digiti minimi induced by means of RdA at rest (the first dorsal interosseous: 24.30⫾1.68 ms; the abductor digiti minimi: 24.29⫾1.62 ms) was significantly slower than that induced using RdB (the first dorsal interosseous: 23.17⫾1.49 ms; the abductor digiti minimi: 23.32⫾1.71 ms) (the first dorsal interosseous: t(19)⫽9.05, P⬍0.0001; the abductor digiti minimi: t(19)⫽4.89, P⫽0.001). The resting motor threshold of RdA (70.75⫾12.68%) was significantly higher than that of RdB (55.35⫾10.99%) (t(19)⫽11.36, P⬍0.0001). A paired t-test was used to evaluate the difference in the MEP increase ratio between the first dorsal interosseous and abductor digiti minimi, which suggests the strength of the MEP facilitation induced by the illusion condition compared with that induced in the resting condition. The increase ratio of the MEP induced from the first dorsal interosseous (1.97⫾1.10) was significantly larger than that from the abductor digiti minimi (1.42⫾0.87) (t(19)⫽2.41, P⫽0.026). In post-experiment interviews, the subjects commented as follows: In the illusion condition, they felt strongly as if their own finger was actually moving. In the non-illusion condition, however, they clearly recognized that their own finger was relaxed while someone else’s finger was abducting on the screen. More or less, all of the subjects answered that they felt as if their own hand was passively moving in the illusion condition. The average response on VAS for this condition was 55.2⫾ 17.4 mm. Experiment 2 MEP amplitudes recorded from the first dorsal interosseous and abductor digiti minimi in each condition are presented in Fig. 4. There was a significant main effect for the “condition” factor (F3,5⫽3.95, P⫽0.029) among the five conditions for MEP recorded from the first dorsal interosseous. On the other hand, MEP amplitudes recorded from the abductor digiti minimi showed no significant effect for the “condition” factor (F3,5⫽2.59, P⫽0.091). In the post hoc test, the MEP
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Fig. 2. Superimposed MEP specimen records induced using RdB during the four conditions from one subject each belonging to group A (A) and group B (B) in experiment 1.
amplitude recorded from the first dorsal interosseous during index-abd was significantly larger than those during all another conditions (P⬍0.05). Though MEP amplitude in the first dorsal interosseous induced in the index-abd condition was significantly facilitated compared with that in the resting condition, there was no significant facilitation of MEP response in the other three control conditions (indexadd, little-abd, little-add). The results of VAS interviews to evaluate introspective responses showed that a significantly strong illusory feeling was induced during movement of the index finger compared with the movement of the little finger (VAS of the index finger movement, 76.7⫾12.2 mm; VAS of the little finger movement, 52.8⫾23.4 mm; t(5)⫽4.11; P⫽0.009). There was no definitive correlation between VAS and increase ratio on MEP (Rho⫽⫺0.36, P⫽0.425).
DISCUSSION The most important point in the present study was whether there was a significant difference in MEP facilitation between the conditions of illusion and non-illusion in experiment 1. The essential difference that those two conditions
represent is the presence or absence of an introspective kinesthetic illusion during task execution, though both the illusion and non-illusion conditions have the element of observing biological action. According to the results of VAS interviews in experiments 1 and 2, the illusory visual stimulus gave subjects the distinct impression that their own fingers were actually moving even though the subjects’ hands were actually stationary. The present results in experiment 1 showed significant facilitation of MEP under the illusion condition compared with that under the non-illusion condition, which was conducted as a control condition. On the other hand, MEP during non-illusion was not significantly facilitated compared with that during the resting and sham conditions, although the average value during the non-illusion was generally higher than that during the resting and sham conditions. This absence of significance does not contradict the previous studies showing that simply observing action facilitated MEP (Fadiga et al., 1995; Gangitano et al., 2004; Maeda et al., 2001, 2002; Strafella and Paus, 2000). Based on the experience-dependent modulation of corticospinal excitability during action observation (Maeda et al., 2001, 2002), the moving hand orien-
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Fig. 3. Average⫾S.D. of MEPs recorded from the first dorsal interosseous (A) and abductor digiti minimi (B) during the four conditions of experiment 1. MEP elicited in the illusion condition was significantly greater than that in the resting and sham conditions for both RdA and RdB, and also greater than that in the non-illusion condition for RdB. (* Indicates the Tukey-Kramer test with a significant level of P⬍0.05.)
tation in this experiment might be not sufficient to facilitate MEP in a non-illusion condition. While facilitation of MEP in an observer by someone else’s hand oriented in a position directed toward the subject’s body has been reported (Maeda et al., 2001, 2002), the hand orientation during the non-illusion condition in this study was directed away from the subject’s body. We speculate that the inappropriate hand orientation in the non-illusion condition may have caused the absence of marked MEP facilitation during the non-illusion condition although the hand orientation adopted for the non-illusion condition corresponded with that used during the illusion condition. Montagna et al. (2005) reported that motor excitability was changed during the observation of a meaningful hand movement executed by someone else, but the orientation of the observed hand in our movie did not correspond to the experience of the observer in their experiment. That the finger movement in the movie of our study was meaningless may be one of the reasons why the non-illusion condition did not facilitate
MEP amplitude. Furthermore, the fact that the subjects could see their actual static hand below the movie might be the most important reason. The previous research have reported that the cortical motor areas are activated during kinesthetic illusory feeling induced by tendon vibration (Naito et al., 1999, 2002, 2005, 2006; Romaiguere et al., 2003, 2005; Naito, 2004; Naito and Ehrsson, 2001, 2006; Casini et al., 2006). In opposition to the kinesthetic illusion effect of the tendon vibration, we clarified that the kinesthetic illusory feeling carried from our experimental visual input induces a facilitatory effect on corticomotor pathways including cortical motor areas, although there was no mechanical input to the muscle spindle. Activation of the abductor digiti minimi, which is the synergistic muscle of the first dorsal interosseous that opens the hand, was not significantly affected by observation of movement by the index finger or little finger. The results of a direct comparison of MEP facilitation (the increase ratio) between the first dorsal interosseous and
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Fig. 4. Average⫾S.D. of MEPs recorded from the first dorsal interosseous and abductor digiti minimi during the five conditions of experiment 2. In index-abd (the “illusion” condition in experiment 1), the MEP recorded from the first dorsal interosseous was significantly greater than those in all another conditions. There was no statistical significance of the MEP amplitude from the abductor digiti minimi.
abductor digiti minimi showed that the extent of facilitation of MEP was obviously greater in the first dorsal interosseous than that in the abductor digiti minimi. This result indicates that, as expected, the effect of the illusion was stronger to the same muscle in the observer as that observed moving on the screen than the synergistic muscle. However, MEP facilitation during the illusory condition does not seem to be common for all body parts. The results of experiment 2, in which MEP facilitation was shown only in the first dorsal interosseous during indexabd, while little-abd did not affect the facilitation to the abductor digiti minimi, support the body-part dependence of the effect of the illusory condition. This contradiction of the effects of the illusory condition on MEP facilitation between the movements by the index finger and little finger may be caused by the strength of the visuomotor relationship or visual experience, since the frequency of seeing index finger movement in daily living is surely higher than that of little finger movement. This point is a prospective research subject. The finding of the present research is that the kinesthetic illusory feeling induced by a visual stimulus and MEP facilitation was stronger in the case of the index finger than in that of the little finger. In experiment 2, MEP induced in the first dorsal interosseous during the illusory condition did not change in the index-add condition. This result indicates that the effect of the illusory condition on corticomotor excitability, which corresponds to the cortical portion that drives the first dorsal interosseous, is dependent on the movement direction. In this point, a function of the mirror neuron network was reported as the presence of a strict temporal coupling between the corticospinal excitability and the dynamics of movements has been reported (Gangitano et al., 2001; Nishitani and Hari, 2000; Oouchida et al., 2004; Terao and Ugawa, 2002), though a relevancy to the present results was unknown.
The moving text observation in this experiment (sham condition) did not induce any significant effects in either the first dorsal interosseous or abductor digiti minimi. This result may support the suggestion that the facilitative visual input on a screen must be an action executed by a human figure (Tai et al., 2004). Introducing kinematic laws of biological movement into the movie may have facilitated the illusion. On the other hand, the facilitatory effect of the illusory condition on corticomotor pathways indicates that even an intransitive meaningless movement in humans can activate the motor output system, whereas such a movement does not activate mirror neurons in monkeys (Rizzolatti, 2005; Rizzolatti and Craighero, 2004). The dominance of vision with respect to body image recognition associated with somatosensory information was confirmed by Botvinick and Cohen (1998), although their experimental condition was only a resting one. They reported that the subjects experienced an illusion of tactile perception in which they felt touch at the locus of a rubber arm. This rubber-arm illusion reveals that a three-way interaction between vision, touch and proprioception creates the illusion of tactile perception. According to other authors who replicated their experiment, the displacement of tactile sensations and the illusion of ownership disappear if the rubber arm is not properly aligned with the subject’s body (van den Bos and Jeannerod, 2002). In the present study’s illusion condition, accurate manipulation of the alignment between actual body and displayed body was a key condition for making the subjects feel the kinesthetic illusion from the visual input. Furthermore, kinematic information from an observed movie seemed to be a key point for observers to distinguish whether the performer in the movie is one’s self or someone else (Daprati et al., 2007). Because the index and little fingers in our movie were passively moved by our experimental device at
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constant angular velocity (isokinetic), there was no individual kinematic property to those movements in the movie. The absence of the properties of active finger movement in the movie may have helped induce the illusory feeling by allowing the subject to forget that he was not the owner of the fingers in the movie. The illusion condition in the present study was novel. The visual stimulus, which was carried in the study of Tardy-Gervet et al. (1982, 1984) was that the background figure shown under the subject’s hand was moved when the subject was seeing his own hand and ambient circumstances through a pinhole. The conditions of Ramachandran et al. (1995, 1996) and Giraux and Sirigu (2003) seem markedly similar to the illusion condition in this study, but the amputee patients also observed their own hand movements. The point of contrast with our research is that the subjects in these prior studies actually observed their own hands. Furthermore, there was voluntary movement on opposite sides in the Ramachandran et al. report. That the manner of the present visual stimulus could induce MEP enhancement suggests that an introspective kinesthetic illusion can be induced under a visual condition, without voluntary motor output from the opposite side or an actual picture of one’s own hand. In terms of clinical relevance, the present approach may offer the possibility of having applications for neuro-rehabilitation since this approach can be interpreted as “passive visual motor imagery.” It is known that an electrical current delivered by means of a circular coil positioned flat at the vertex can activate the motor cortex preferentially when the induced current flows from back to front, or non-preferentially when the current in the brain flows from front to back (Trompetto et al., 1999). In RdA, the coil current flows counterclockwise, so that the current induced in the brain flows clockwise. On the contrary, when the RdB is placed on the skull, the current induced in the brain is counterclockwise. TMS in this case induces MEP preferentially to record from a muscle in the left side. Different neural circuits having different motor thresholds and MEP latencies are recruited depending on which side of the coil faces up (Day et al., 1989; Wilson et al., 1996; Trompetto et al., 1999; Terao and Ugawa, 2002). The present results showed that MEP latency induced at rest by means of RdA was significantly longer than that induced by RdB and that the resting motor threshold induced by RdA was significantly higher than that induced by RdB. The absence of MEP amplitude differences between MEPs induced by RdA and RdB as shown in the present results suggests that the facilitatory effect carried over from a visual input affected both neuronal chains.
CONCLUSION In conclusion, a new finding in the present study is that, first, the kinesthetic self-movement illusion can be induced by our experimental condition in which a video of a moving finger was shown with the display situated so that the video hand overlaps closely with the subject’s actual hand. Second, the illusion condition causes a measurable physiolog-
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ical effect (facilitatory effect of input to corticomotor pathways), though the facilitatory effect was shown only when the index finger was abducting in the video from the agonist muscle first dorsal interosseous. These findings mean the kinesthetic illusion is not just a process of movement recognition but also has a functional role of modulating excitability in corticomotor pathways. We think that there is a value to ascertaining whether our experimental method using video is as effective as the rehabilitation intervention to facilitate recovery of motor function, for example in a stroke patient.
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(Accepted 21 July 2007) (Available online 1 August 2007)