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Article

Impact of Visual Kinesthetic Illusions on Reciprocal Inhibition and Motor Function

Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Niigata 950-3198, Japan
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(24), 11725; https://doi.org/10.3390/app142411725
Submission received: 24 October 2024 / Revised: 27 November 2024 / Accepted: 12 December 2024 / Published: 16 December 2024

Abstract

:
Reciprocal inhibition is often diminished in elderly individuals and those with upper motor neuron disorders. This reduction in reciprocal inhibition can hinder smooth joint movement. For subjects who have increased muscle tone and a limited range of motion in the joints, we focused on visual kinesthetic illusions as an intervention to increase reciprocal inhibition. We aimed to investigate the effects of visual kinesthetic illusions on reciprocal inhibition and motor function in the ankle joint. Participants participated in two experiments measuring reciprocal inhibition, namely reciprocal Ia inhibition and D1 inhibition, as well as motor functions related to ankle dorsiflexion and plantar flexion. Visual kinesthetic illusion was induced by displaying an image of each subject’s foot on a monitor. Our results showed that the visual kinesthetic illusion enhanced D1 inhibition and improved motor function in the ankle joint by prioritizing agonist muscle activity. We also observed a correlation between reciprocal inhibition and the muscle activity ratio. These findings suggest that visual kinesthetic illusions may improve motor function by increasing reciprocal inhibition. This study is the first to demonstrate the effects of visual kinesthetic illusion on reciprocal inhibition, and we believe that these findings can be applied in rehabilitation.

1. Introduction

Reciprocal inhibition (RI) is crucial in facilitating smooth joint movement. Research has indicated that inhibitory interneurons in the spinal cord contribute to RI [1,2]. Peripheral inputs and the activity of supraspinal regions, including the primary motor cortex (M1) and supplementary motor cortex, modulate the interneurons, contributing to RI [3,4,5,6,7,8]. Previous studies have indicated that RI declines in individuals with upper motor neuron disorders or older adults [9,10]. A reduction in RI results in joint movement issues due to the co-contraction of opposing muscles, negatively impacting walking and balance capabilities [11].
Repetitive passive movement (RPM) is a technique used to enhance RI. This intervention involves executing repetitive, passive motions on the targeted joints. Our research team has identified optimal RPM parameters for the ankle joint: a higher angular velocity (40°/s < 160°/s) and a broader range of motion (20° < 40°) [12]. Our research demonstrates that focusing attention on the RPM intervention site prolongs the after-effect on RI compared to not directing attention there [13]. Also, focusing attention on the RPM intervention site during RPM reduces the activity of intracortical inhibitory circuits, including short latency afferent inhibition (SAI) [14], and increases motor evoked potential (MEP) [15], which indicates corticospinal tract excitability. However, while it is necessary to bolster RI, RPM may not deliver the intended intervention results for patients who face limitations relating to its use, such as spasticity and restricted range of motion caused by upper motor neuron disorders, spinal cord injuries, and aging. In particular, in clinical settings, patients suffering from upper motor neuron disorders and spinal cord injuries and older individuals requiring RI enhancement due to diminished RI function may experience limited joint mobility stemming from excessive spasticity or joint contractures. Consequently, they might find it challenging to receive RPM with effective intervention parameters, leading to a lack of anticipated benefits.
Sensory input manipulation can induce the experience of body illusion [16]. One specific type of illusion, known as visual kinesthetic illusion, occurs when an individual at rest perceives bodily movement or feels the urge to move a body part while observing a video of that part in motion [17,18]. The body illusion enhances motor cortex excitability by decreasing SAI [19,20,21]. Moreover, the visual kinesthetic illusion of ankle joint movement reportedly increases corticospinal tract excitability [22]. We consider that visual kinesthetic illusion enhances M1 excitability and promotes the activation of RI’s inhibitory interneurons by descending the input, thereby improving RI performance.
We herein aimed to explore how visual kinesthetic illusion impacts RI and ankle joint motor function. We hypothesized that visual kinesthetic illusions boost the activation of inhibitory interneurons of RI via descending input, which results from heightened M1 excitability, thereby enhancing RI. Enhancement of RI is also expected to diminish co-contraction between antagonistic muscles and improve ankle joint motor function.

2. Methods

2.1. Participants

This study involved 18 healthy adults (average age 22 ± 0.9 years; height 165 ± 6.9 cm; weight 54 ± 7.3 kg; with nine females). The sample size calculation was calculated using G-Power Software (version 3.1.9, Universität Düsseldorf, Germany). Considering a significance level of 5% and a power of 80%, 18 participants were included to satisfy the sample size requirements. Individuals with a history of orthopedic disease in the lower limbs, central nervous system conditions, psychiatric disorders, or on psychiatric medications were excluded. Participants were informed about the study’s purpose and their rights. All participants provided written informed consent before the commencement of the study. This study was approved by the university’s ethics committee (18267-190918) and was conducted following its ethical standards and the 1964 Declaration of Helsinki, along with its subsequent amendments.

2.2. Measurement Position

In experiment 1, measurements were taken from the right limb, and the participants sat in a chair with a hip flexion of 90°, knee flexion of 60°, and ankle plantar flexion of 20° [12,23]. In experiment 2, participants sat in a chair with their hips flexed at 90°, knees at 60°, and ankles at 30° of plantar flexion. To ensure consistent measurement positions during the experiment, their lower limbs were secured to the seat at the thighs and the footplate (Takei Scientific Instruments, Niigata, Japan).

2.3. Electromyography (EMG)

We used Ag/AgCl electrodes (Blue Sensor, METS, Tokyo, Japan) for surface electromyography. Participants were instructed to lie in a prone position on a bed and perform ankle plantar flexion with their knees bent to identify the soleus muscle (Sol). To identify the tibial anterior muscle (TA), participants were instructed to lie in a supine position on a bed and perform ankle dorsiflexion. Before the application of electrodes, the skin at the site was cleaned to minimize electrical impedance. EMG electrodes were then placed on the belly of the right TA and right Sol, adhering to SENIAM guidelines [24]. Electrodes were attached perpendicularly, causing them to cross the muscle fibers. The electrodes were spaced 20 mm apart. A ground electrode was placed between the stimulating electrodes and the recording electrode of the TA. Electromyographs were filtered with a 10–1000-Hz band-pass filter and amplified 100 times using an amplifier (FA-DL-720-140, 4Assist, Tokyo, Japan). These signals were digitally recorded on a personal computer at a sampling rate of 10 kHz for offline analysis. Data analysis was performed using PowerLab 8/30 (AD Instruments, Colorado Springs, CO, USA) and LabChart 7 (AD Instruments).

2.4. Electrical Stimulation

An electrical stimulation device (SEN-8203; Nihon Kohden, Tokyo, Japan) and an isolator (SS-104J, Nihon Kohden, Tokyo, Japan) were used to deliver the stimulation. A bipolar electrode was placed on the common peroneal nerve beneath the fibula head to stimulate the TA during the conditioned stimulation. We closely examined the electrode’s positioning to avoid activating the peroneus muscle [13]. In the test stimulus, the anode and cathode were positioned on the upper patella and popliteal region, where stimulation of the tibial nerve elicited the Sol H-reflex and M waves.

2.5. RI Measurement

RI measurements were conducted following previous studies [1,13,25,26]. RI evaluated the pathway that inhibits spinal anterior horn cells of the Sol from nerves innervating the TA by applying a test stimulus to the tibial nerve following a conditioned stimulus to the common peroneal nerve. Stimulation of the common peroneal nerve reduces the excitability of spinal anterior horn cells in the soleus muscle through inhibitory interneurons. Consequently, applying a test stimulus to the tibial nerve after the conditioning stimulus is anticipated to lower the H-reflex amplitude in the soleus. We used 1-ms square wave stimuli, setting the intensity at the M wave threshold (M wave amplitude less than 100 µV) of the TA for the conditioned stimuli and 15–25% of the maximal upper stimulus (Mmax) amplitude of the Sol H-reflex for the test stimuli. Maintaining constant stimulation intensity eliminates the influence of electrical stimulation intensity during RI measurement. The three stimulation conditions included conditioning stimulation–test stimulation intervals (CTIs) of either 2 ms (CTI 2 ms) or 20 ms (CTI 20 ms) alongside a test stimulus administered without a preceding conditioning stimulus (single) [13]. Previous studies have reported that the CTI 2 ms produces the largest amount of reciprocal Ia inhibition due to disynaptic inhibition involving the reciprocal Ia inhibitory interneuron [1,27]. In contrast, a CTI of 20 ms results in the largest amount of D1 inhibition, which stems from presynaptic inhibition associated with the primary afferent depolarization (PAD) interneuron [1]. Every stimulus condition was tested randomly 12 times at a frequency of 0.3 Hz, leading to 36 stimuli in each measurement set. Since H-reflex stabilizes after the third stimulus, a minimum of three stimuli were required before starting any measurements [28].

2.6. Motor Function Assessment

We evaluated motor function by executing a single cycle of ankle movement between 30° of plantar flexion and 10° of dorsiflexion, then returning. Before measuring the motor function, we recorded the muscle activity of the TA and Sol during each subject’s maximum voluntary contraction (MVC). Subjects were seated with their arms crossed over their chests and instructed to initiate the motor task with maximum effort immediately following the examiner’s signal. Each task was repeated three times per set, with a 10-s rest between trials.

2.7. Visual Kinesthetic Illusion

We filmed each subject’s right foot to create the visual kinesthetic illusion. The foot was filmed at the ankle joint while resting at 20° of plantar flexion before filming the foot while RPM. To provide the most effective RPM parameter, we chose an angular velocity of 160 °/s, with a motion range from 30° plantar flexion to 10° dorsiflexion [12,23]. The camera’s position remained fixed during filming, and the foot size displayed on the monitor was adjusted to match each subject’s foot size. Videos were filmed at least two days before the experiment, considering that RPM might influence the central nervous system.
The two intervention conditions included a sham condition and an illusion condition. In the sham condition, participants were asked to concentrate on their resting foot, which was shown on the monitor. Conversely, in the illusion condition, they focused on their foot receiving RPM that was displayed on the monitor to create the visual kinesthetic illusion. The intervention videos were set to alternate between foot visuals and black screens using Tobii Pro Lab software (version 1.181.37603, Tobii, Danderyd, Sweden). These were displayed on a 15.6-inch monitor (EX-LDC161DBM, I-O DATA DEVICE, Ishikawa, Japan), with its position adjusted using a monitor arm. A previous study indicated a positive correlation between perceived visual kinesthetic illusion levels and corticospinal tract excitability [22]. Participants were instructed to place the monitor above their knee joint with their hand, aligning it with the size and position of their foot. Before the intervention, they were directed to focus solely on the ankle joint movement shown in the video. The intervention lasted 10 min to sustain participant concentration, comprising 10 sets of 50 s of the foot video presentation, each followed by a 10-s break displaying a black screen.

2.8. Assessment of the Visual Kinesthetic Illusion

Based on previous research, assessments were conducted immediately after the intervention of the degree of the visual kinesthetic illusion, termed “vividness”. Participants responded to the following question: “While watching the video, did you feel as if your legs were moving?” Their ratings ranged from −3 to +3, where −3 meant “strongly disagree”, −2 “disagree”, −1 “somewhat disagree”, 0 “neither agree nor disagree”, +1 “somewhat agree”, +2 “agree”, and +3 “strongly agree” [17,18].

2.9. Gaze Analysis

In this study, a gaze analysis device (Tobii Pro Nano, Danderyd, Sweden) was used to ensure participants focused on the monitor throughout the intervention. The device was mounted at the lower edge of the monitor and had a sampling rate of 60 Hz. Following a 10-s calibration across five designated points, participants were instructed to track a white dot moving among nine locations on the screen. The intervention video began after the examiner provided instructions related to the intervention.

2.10. Experimental Protocol

In experiment 1, we measured the RI. Before this, we set the intensity of electrical stimulation for both the conditioning and test stimuli. RI was measured before (Pre), immediately after (Post), 5 min (Post 5), and 10 min (Post 10) after the intervention (Figure 1a). In experiment 2, we evaluated motor functions to explore the impact of the visual kinesthetic illusion. The motor task at Pre was recorded after measuring each subject’s MVC, followed by a 5-min rest. Motor function was assessed at Pre, Post 0, and Post 10 (Figure 1b). Each intervention lasted 10 min. We randomly assigned the two intervention conditions for each experiment, ensuring at least two days between condition applications.

2.11. Data Analysis

2.11.1. Experiment 1

In experiment 1, we analyzed the Sol H-reflex amplitude and Mmax. The Sol H-reflex amplitude was determined by averaging the peak-to-peak values of the waveform, excluding the maximum and minimum values for each condition. To compare the different intervention conditions, we calculated the Sol H-reflex amplitude as a percentage of the Sol Mmax amplitude ([Sol H-reflex amplitude/Sol Mmax amplitude] × 100: % Mmax). To compare changes over time in each intervention, we divided the H-reflex amplitude for the test stimulus paired with the conditioned stimulus by the H-reflex amplitude for the test stimulus alone, representing this as a percentage ([amplitude of conditioned H-reflex amplitude/test H-reflex amplitude] × 100: % test H-reflex). The change in H-reflex amplitude at a CTI of 20 ms was calculated by subtracting the Post value from the Pre value.

2.11.2. Experiment 2

The analysis interval was segmented into phases based on joint angle. The dorsiflexion phase (DF) was defined as the time from the start of ankle dorsiflexion to its end. The plantar flexion phase (PF) was defined as the period from the end of dorsiflexion to the offset of plantar flexion. The total range of motion (Total) was defined as the timeframe from the beginning of DF to the end of PF. Each analysis item calculated for each analysis interval included the EMG, which processed the full wave rectified average muscle activity of TA and Sol, execution time, and rate of joint development (RJD). In addition, during the DF, we measured peak torque, electromechanical delay (EMD), and EMG during EMD.
The muscle activity ratio was determined by dividing the muscle activity of TA by that of Sol. Muscle activity during the MVC was determined by averaging the full-wave rectified signal over the most stable 1-s period of a 3-s isometric contraction [13,29]. In addition, the percentage of MVC during the motor task was calculated by dividing each participant’s muscle activity by their MVC value. The onset of execution time was defined as when the joint angle shifted by 1°, and the offset was noted when the joint angle reverted to 30° of PF. RJD was calculated by dividing the range of motion in each phase by the movement duration for that phase. Each analysis item in Total was achieved by averaging the values of DF and PF. The EMD was defined as the duration from the onset of TA EMG to the activation of dorsiflexion torque, with both events identified when they surpassed the mean by more than three standard deviations. The change in the muscle activity ratio was determined by taking the difference between the Post 10 and Pre values. For Sol %MVC, the change was calculated by subtracting the Pre value from the Post 10 value.
In experiments 1 and 2, the gaze analysis used Tobii Pro Lab software (Tobii, Danderyd, Sweden). The complete monitor surface served as the area of interest (AOI). The analysis item was the total time spent in the AOI.

2.12. Statistical Analysis

Normality for each item was determined using the Shapiro–Wilk test. In experiment 1, repeated measures three-way ANOVA was conducted to evaluate the interaction among intervention condition (sham and illusion), stimulus condition (single, CTI 2 ms, and CTI 20 ms), and measurement time (Pre, Post 0, Post 5, and Post 10). For post hoc analysis, Bonferroni correction along with paired t-test was used to compare the stimulus conditions within each intervention condition. In experiment 2, a repeated measures two-way ANOVA was used to assess the intervention conditions (sham and illusion) across measurement times (Pre, Post 0, and Post 10). Bonferroni-corrected multiple-comparison tests were used for post hoc analysis. The effect size was presented as partial η2 from repeated measures ANOVA and quantified as small (0.0099), middle (0.0588), and large (0.1379) [30]. In addition, Spearman’s rank correlation coefficient was calculated to explore the relationships in the data. The significance level was set at 5% for all analyses.

3. Results

3.1. Reciprocal Inhibition

The Sol background EMG, Sol Mmax amplitude value, and TA M wave amplitude value are shown in Table 1, Table 2 and Table 3, respectively. Representative raw data of the Sol and TA waveforms are shown in Figure 2.
The results of repeated measures three-way ANOVA did not reveal a main effect of the intervention condition [F(1, 17) = 0.921, p = 0.351, partial η2 = 0.051] or measurement time [F(3, 51) = 0.047, p = 0.987, partial η2 = 0.003]; however, a main effects of the stimulus condition [F(2, 34) = 60.751, p = 0.001, partial η2 = 0.781] and the interaction of the three factors [F(6, 102) = 3.243, p = 0.006, partial η2 = 0.160] were observed. The H-reflex amplitude values at the measurement times under CTI 2 ms and CTI 20 ms were compared with the values at Pre. In CTI 2 ms, both the sham and illusion conditions did not show a significant difference in the H-reflex amplitude compared with Pre (Figure 3a,c). In CTI 20 ms, the H-reflex amplitude value under the sham condition did not significantly differ from Pre (Figure 3b), but that under the illusion condition was significantly lower at Post 10 than at Pre (p = 0.036, Figure 3d).
There was no notable variation in the H-reflex amplitude value during the single condition at each measurement time across both intervention conditions (Table 4). Consequently, the stimulation achieved a consistent H-reflex amplitude value in both intervention conditions.

3.2. DF and EMG

The repeated measures two-way ANOVA results for EMD revealed no main effect of the intervention condition [F(1, 17) = 0.196, p = 0.664, partial η2 = 0.011] or measurement time [F(2, 34) = 0.928, p = 0.405, partial η2 = 0.052]. However, a interaction between these two factors was identified [F(2, 34) = 3.404, p = 0.045, partial η2 = 0.167]. The post hoc test showed no significant differences in EMD (Figure 4A).

3.3. PF

The muscle activity ratio analysis for PF revealed that the repeated measures two-way ANOVA did not indicate a main effect of measurement time [F(2, 34) = 1.913, p = 0.163, partial η2 = 0.101]. However, it did show a main effect for the intervention condition [F(1, 17) = 10.429, p = 0.005, partial η2 = 0.380], as well as an interaction between the two factors [F(2, 34) = 6.453, p = 0.004, partial η2 = 0.275]. Post hoc testing revealed that the illusion condition was significantly lower than the sham condition at Post 10 in PF (p = 0.026, Figure 4B).

3.4. Total

The repeated measures two-way ANOVA results showed no main effect of the intervention condition, timing of measurement, or their interaction (Figure 4C).

3.5. Relationship Between Changes in D1 Inhibition and Motor Function Improvement

In the illusion condition, we observed a significant positive correlation between the change in the H-reflex amplitude at CTI 20 ms and the change in the muscle activity ratio during EMD (p = 0.021, r = 0.544, Figure 5a,b). In addition, in the illusion condition, a significant negative correlation was observed between the change in the H-reflex amplitude at CTI 20 ms and the change in Sol %MVC during EMD (p = 0.015, r = −0.573, Figure 5c,d).

3.6. Total Visit Time to the AOI

The gaze analysis revealed that the total visit duration was 479.5 s in the sham condition and 481.2 s in the illusion condition.

4. Discussion

This study examined whether the visual kinesthetic illusion regarding RPM can enhance RI and improve ankle joint movement function. The main findings were that the visual kinesthetic illusion enhanced D1 inhibition, which caused a reduction in the activity of the antagonist muscle.

4.1. Effect on RI

In this study, in the sham condition, participants observed a video of their resting foot on the monitor. The findings from the sham condition demonstrated that watching the resting foot video did not affect RI.
The results of experiment 1 revealed that the visual kinesthetic illusion related to RPM improved D1 inhibition. This body illusion is known to generate the feeling of the body shifting from its initial position, attributed to the alignment of visual perception with somatosensory input from the body [31]. In this situation, a conflict arises between the body position sensed through visual input and that felt through somatosensory input. During the body illusion, this inconsistency is thought to be alleviated by a reduction in somatosensory input [20,32,33]. Adjusting somatosensory input has been shown to influence M1 through afferent inhibition [34]. The SAI reportedly decreases due to body illusion [20]. In support of the attenuation of SAI due to body illusions, a previous study demonstrated that visual kinesthetic illusion increases corticospinal tract excitability [22]. This indicates that visual kinesthetic illusions may lead to disinhibition in M1, increasing its excitability. Previous studies have shown how M1 excitability affects RI [5,35]. Transcranial direct current stimulation (tDCS) is a noninvasive method that modifies cortical activity beneath the electrode based on polarity. When a cathodal electrode is used, it diminishes the cortical excitability at the stimulation site. RI decreases with the application of a cathodal electrode on M1 [35]. Repetitive transcranial magnetic stimulation (rTMS) similarly modulates cortical activity. A previous study showed that increasing M1 excitability enhanced RI. This enhancement is believed to occur via a descending input from M1, which affects the activity of RI interneurons [36]. Thus, it is proposed that the visual kinesthetic illusion boosts M1 excitability and enhances RI by stimulating the inhibitory interneurons of RI via descending signals from supraspinal control.
The results of this study revealed that the visual kinesthetic illusion enhanced D1 inhibition within the RI. D1 inhibition is believed to occur via presynaptic inhibition, in which PAD interneurons inhibit input from antagonist muscle Ia fibers [1]. Additionally, presynaptic inhibition selectively reduces sensory input, unlike postsynaptic inhibition [4]. Cutaneous afferent reflex, identified as a reflex triggered by sensory signals, is reportedly diminished by descending input from the corticospinal tract during voluntary movement. This descending input stimulates the PAD interneurons, leading to presynaptic inhibition [37]. A previous study revealed that increasing M1 excitability enhances presynaptic inhibition but does not affect postsynaptic inhibition [5]. The visual kinesthetic illusion associated with RPM might increase excitability in the corticospinal tract by enhancing M1 activity. This elevated activity can decrease sensory input through presynaptic inhibition, thereby enhancing D1 inhibition.

4.2. Motor Function

The results of experiment 2 indicated that enhancing D1 inhibition through the visual kinesthetic illusion improves motor function, particularly to reduce the activity of the antagonist’s muscles. This study showed that the visual kinesthetic illusion related to RPM influenced spinal and motor functions.
In the EMD, correlations between the change in muscle activity and the change in the enhancement of D1 inhibition were observed. This implies that the visual kinesthetic illusion enhances RI, reducing the excessive co-contraction of the antagonist muscles and enabling smoother joint movement. RI aids in achieving fluid joint movement by inhibiting the stretch reflex of the antagonist muscle at the start of movement [9]. A previous study examined whether ankle dorsiflexion function improved after RPM and revealed that enhancing RI favored TA muscle activity [13]; these findings were consistent with those of the present study. As a factor of this improvement, RI would inhibit the stretch reflex on antagonist muscle. The spinal cord excitability of Sol begins to decline as TA muscle activity occurs on dorsiflexion. Conversely, Sol’s spinal cord excitability reportedly increases approximately 60 ms after TA muscle activity begins [38]. Sol spinal cord excitability enhancement is believed to result from a stretch reflex in the triceps surae. The present study suggested that as the RI increased, the stretch reflex of the antagonist muscle Sol diminished at beginning joint movement, causing a further reduction in Sol muscle activity.
Sol significantly dominated muscle activity in PF due to the visual kinesthetic illusion. This finding indicates that, similar to dorsiflexion EMD, the visual kinesthetic illusion of RPM largely influences muscle activation during plantar flexion, making agonist muscles predominant. This phenomenon may stem from enhanced RI adjustment functions caused by the visual kinesthetic illusion. During plantar flexion, the RI from TA to Sol decreases due to descending inputs from supraspinal control on RI interneurons [9]. Consequently, plantar flexion increases the excitability of alpha motor neurons in the Sol, leading to increased activation of the Sol muscle. The current research assessed the RI from the TA to the Sol. However, it is important to note that RI also occurs from the Sol to the TA in vivo, with evidence suggesting that this inhibition is more pronounced than that from the TA to the Sol [39]. The strong inhibition from Sol to TA is thought to prevent hindrance in the muscle activity of the triceps surae, an antigravity muscle. The present study indicated that the visual kinesthetic illusion enhanced the modulatory function of RI and increased alpha motor neuron excitability in the Sol during PF. Moreover, this modulatory function may be more pronounced in the Sol, which is more susceptible to the effects of RI.

4.3. Clinical Applications

This study proposes that the visual kinesthetic illusion involving RPM can serve as an intervention to enhance motor function decline linked to reduced RI. This technique is advantageous because it does not necessitate actual joint movements, suggesting potential for broader application with patients and flexible intervention timing. Additionally, this illusion might also be utilized as a virtual reality intervention. Future studies should explore whether spinal cord and motor function improvements are possible for patients experiencing decreased RI.

4.4. Limitations

This study had two limitations. First, RI and motor function had to be assessed on separate days since voluntary contractions can influence the central nervous system’s activity via peripheral inputs. Second, measurements were taken up to 10 min post intervention in both experiments 1 and 2. Previous studies have shown immediate changes in corticospinal tract excitability following the visual kinesthetic illusion, prompting us to concentrate on our measurements right after the intervention. However, our study noted increased RI due to the visual kinesthetic illusion 10 min after the intervention. As the duration of this RI increase remains uncertain, future research should evaluate it over a more extended period following the intervention.

5. Conclusions

This study explored whether the visual kinesthetic illusion regarding RPM enhances RI and improves motor function. The findings indicated that the visual kinesthetic illusion improved RI 10 min post intervention. In addition, regarding motor function, we found that joint movement improved through the preferential activation of agonist muscles. Future research should focus on determining if stroke patients and elderly individuals with diminished RI show improvements in either area.

Author Contributions

Conceptualization T.O. and R.H.; Data curation T.O. and R.H.; Formal analysis R.H.; Funding acquisition R.H.; Investigation T.O.; Methodology T.O., R.H., N.S., H.Y., C.S., T.I., M.K., K.S. and M.E.; Project administration R.H.; Resources R.H. and M.E.; Software R.H.; Supervision R.H. and M.E.; Validation T.O. and R.H.; Visualization T.O.; Writing—original draft T.O.; Writing—review & editing T.O., R.H., N.S., H.Y., C.S., T.I., M.K., K.S. and M.E. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science [grant number: 22K11323].

Institutional Review Board Statement

The study protocol was approved by the University’s Ethical Review Committee (18267-190918) on 18 November 2019. The experiments were conducted following the ethical standards of the Niigata University of Health and Welfare and the 1964 Declaration of Helsinki and its later amendments.

Informed Consent Statement

Participants were fully informed about the research content and their rights, and written informed consent was obtained from them before the study initiation.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on reasonable request.

Conflicts of Interest

The authors declare no conflict of interest. The sponsors played no role in the study’s design, execution, interpretation, or writing.

Abbreviations

RIReciprocal inhibition
RPMRepetitive passive movement
MEPMotor evoked potential
SAIShort latency afferent inhibition
TATibial anterior
SolSoleus
CTIConditioning stimulation–test stimulation interval
PADPrimary afferent depolarization
DFDorsiflexion phase
PFPlantar flexion phase
RJDRate of joint development
EMDElectromechanical delay
SDStandard deviation
AOIArea of interest
SEStandard error

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Figure 1. Experimental Protocols for measurement in two intervention conditions. Two intervention conditions, sham and illusion, were conducted randomly during the 10-min intervention. In experiment 1, we measured the Sol Mmax and TA motor threshold before the measurement of RI. The stimulation conditions for the measurement of RI were single, CTI 2 ms, and CTI 20 ms. Measurement times were established before the intervention (Pre), immediately after (Post 0), 5 min later (Post 5), and 10 min later (Post 10) the intervention (a). In experiment 2, participants practiced the motor task for measurements of motor function. Before the Pre-measurement, the MVC of Sol and TA was measured. Measurement times were set at Pre, Post 0, and Post 10. Motor tasks were performed three times, with a 30-s rest period between each (b). CTI, conditioning stimulation–test stimulation interval; Sol, soleus muscle; TA, tibialis anterior muscle; MVC, maximum voluntary contraction.
Figure 1. Experimental Protocols for measurement in two intervention conditions. Two intervention conditions, sham and illusion, were conducted randomly during the 10-min intervention. In experiment 1, we measured the Sol Mmax and TA motor threshold before the measurement of RI. The stimulation conditions for the measurement of RI were single, CTI 2 ms, and CTI 20 ms. Measurement times were established before the intervention (Pre), immediately after (Post 0), 5 min later (Post 5), and 10 min later (Post 10) the intervention (a). In experiment 2, participants practiced the motor task for measurements of motor function. Before the Pre-measurement, the MVC of Sol and TA was measured. Measurement times were set at Pre, Post 0, and Post 10. Motor tasks were performed three times, with a 30-s rest period between each (b). CTI, conditioning stimulation–test stimulation interval; Sol, soleus muscle; TA, tibialis anterior muscle; MVC, maximum voluntary contraction.
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Figure 2. Representative raw data tracing. Representative raw data tracing of one participant for the illusion condition. The stimulation conditions were single from top to bottom, with CTI 2 ms (reciprocal Ia inhibition) and CTI 20 ms (D1 inhibition) for the Sol and TA. The 10 waveforms of the Sol H-reflex are shown, and the bold black lines represent the summed averages of the 10 waveforms. The horizontal data show the changes over time before (Pre), immediately after (Post 0), 5 min after (Post 5), and 10 min after (post 10) the intervention. CTI, conditioning stimulation–test stimulation interval; Sol, soleus muscle; TA, tibialis anterior muscle.
Figure 2. Representative raw data tracing. Representative raw data tracing of one participant for the illusion condition. The stimulation conditions were single from top to bottom, with CTI 2 ms (reciprocal Ia inhibition) and CTI 20 ms (D1 inhibition) for the Sol and TA. The 10 waveforms of the Sol H-reflex are shown, and the bold black lines represent the summed averages of the 10 waveforms. The horizontal data show the changes over time before (Pre), immediately after (Post 0), 5 min after (Post 5), and 10 min after (post 10) the intervention. CTI, conditioning stimulation–test stimulation interval; Sol, soleus muscle; TA, tibialis anterior muscle.
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Figure 3. Changes in reciprocal inhibition over time. (a,c) depict the CTI at 2 ms, whereas (b,d) represent the CTI at 20 ms. The top row corresponds to the sham condition, whereas the bottom row indicates the illusion condition. The thin solid lines track changes over time for the 18 participants, whereas the thick solid lines represent the average values. The vertical axis measures the amplitude of the conditioning H-reflex divided by the amplitude of the test H-reflex, multiplied by 100. The horizontal axis outlines time points: before the intervention (Pre), immediately after (Post 0), 5 min after (Post 5), and finally 10 min after (Post 10) the intervention. Bonferroni correction along with paired t-test was used to compare measurement times against Pre. Asterisk indicates values that were significantly different from Pre (* p < 0.05). CTI, conditioning stimulation–test stimulation interval.
Figure 3. Changes in reciprocal inhibition over time. (a,c) depict the CTI at 2 ms, whereas (b,d) represent the CTI at 20 ms. The top row corresponds to the sham condition, whereas the bottom row indicates the illusion condition. The thin solid lines track changes over time for the 18 participants, whereas the thick solid lines represent the average values. The vertical axis measures the amplitude of the conditioning H-reflex divided by the amplitude of the test H-reflex, multiplied by 100. The horizontal axis outlines time points: before the intervention (Pre), immediately after (Post 0), 5 min after (Post 5), and finally 10 min after (Post 10) the intervention. Bonferroni correction along with paired t-test was used to compare measurement times against Pre. Asterisk indicates values that were significantly different from Pre (* p < 0.05). CTI, conditioning stimulation–test stimulation interval.
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Figure 4. (A) Motor function during dorsiflexion phase. (A) displays the results of the motor task during the dorsiflexion phase (DF) and electromechanical delay (EMD). The bar graph illustrates the mean ± standard deviation for each analysis item. The units on each vertical axis are seconds (s) for execution time, the muscle activity ratio between TA and Sol, degrees per second (°/s) for the rate of joint development (RJD), and Newton-meters (Nm) for peak torque (PT) during ankle dorsiflexion. Gray bars represent pre-intervention values (Pre), blue bars indicate values recorded immediately after (Post 0), and orange bars show values taken 10 min later (Post 10). Multiple-comparison tests with Bonferroni correction were performed to evaluate the measurement times against Pre, and among the different intervention conditions. (B) Motor function during plantar flexion phase. (B) displays the results of the motor task during the plantar flexion phase (PF). The bar graph illustrates the mean ± standard deviation for each analysis item. The units on each vertical axis are seconds (s) for execution time, the muscle activity ratio between TA and Sol, and degrees per second (°/s) for the rate of joint development (RJD). Gray bars represent pre-intervention values (Pre), blue bars indicate values taken immediately after (Post 0), and orange bars show values recorded 10 min later (Post 10). Multiple-comparison tests with Bonferroni correction were performed to evaluate the measurement times against Pre, and among the different intervention conditions. * p < 0.05. (C) Motor function during the total phase. In (C), we display the results of the motor task during the total phase. The bar graph illustrates the mean ± standard deviation for each analysis item. The units on each vertical axis are seconds (s) for execution time, the muscle activity ratio between TA and Sol, and degrees per second (°/s) for the rate of joint development (RJD). Gray bars depict pre-intervention values (Pre), blue bars represent values collected immediately after (Post 0), and orange bars indicate values taken 10 min later (Post 10).
Figure 4. (A) Motor function during dorsiflexion phase. (A) displays the results of the motor task during the dorsiflexion phase (DF) and electromechanical delay (EMD). The bar graph illustrates the mean ± standard deviation for each analysis item. The units on each vertical axis are seconds (s) for execution time, the muscle activity ratio between TA and Sol, degrees per second (°/s) for the rate of joint development (RJD), and Newton-meters (Nm) for peak torque (PT) during ankle dorsiflexion. Gray bars represent pre-intervention values (Pre), blue bars indicate values recorded immediately after (Post 0), and orange bars show values taken 10 min later (Post 10). Multiple-comparison tests with Bonferroni correction were performed to evaluate the measurement times against Pre, and among the different intervention conditions. (B) Motor function during plantar flexion phase. (B) displays the results of the motor task during the plantar flexion phase (PF). The bar graph illustrates the mean ± standard deviation for each analysis item. The units on each vertical axis are seconds (s) for execution time, the muscle activity ratio between TA and Sol, and degrees per second (°/s) for the rate of joint development (RJD). Gray bars represent pre-intervention values (Pre), blue bars indicate values taken immediately after (Post 0), and orange bars show values recorded 10 min later (Post 10). Multiple-comparison tests with Bonferroni correction were performed to evaluate the measurement times against Pre, and among the different intervention conditions. * p < 0.05. (C) Motor function during the total phase. In (C), we display the results of the motor task during the total phase. The bar graph illustrates the mean ± standard deviation for each analysis item. The units on each vertical axis are seconds (s) for execution time, the muscle activity ratio between TA and Sol, and degrees per second (°/s) for the rate of joint development (RJD). Gray bars depict pre-intervention values (Pre), blue bars represent values collected immediately after (Post 0), and orange bars indicate values taken 10 min later (Post 10).
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Figure 5. Relationship between Sol H-reflex amplitude changes and motor function. (a,b) show the change of the Sol H-reflex amplitude at CTI 20 ms and the muscle activity ratio during EMD. In the same way, (c,d) represent the changes of Sol H-reflex amplitude at CTI 20 ms and Sol %MVC during EMD. The graph distinguishes between the sham condition, shown in gray, and the illusion condition, represented in orange. The data did not follow a normal distribution, so Spearman’s rank correlation coefficient was applied. CTI, conditioning stimulation–test stimulation interval.
Figure 5. Relationship between Sol H-reflex amplitude changes and motor function. (a,b) show the change of the Sol H-reflex amplitude at CTI 20 ms and the muscle activity ratio during EMD. In the same way, (c,d) represent the changes of Sol H-reflex amplitude at CTI 20 ms and Sol %MVC during EMD. The graph distinguishes between the sham condition, shown in gray, and the illusion condition, represented in orange. The data did not follow a normal distribution, so Spearman’s rank correlation coefficient was applied. CTI, conditioning stimulation–test stimulation interval.
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Table 1. Electromyography (EMG) background for Sol.
Table 1. Electromyography (EMG) background for Sol.
PrePost 0Post 5Post 10
Sham5.2 ± 0.25.5 ± 0.25.1 ± 0.15.2 ± 0.1
Illusion4.9 ± 0.24.6 ± 0.28.1 ± 3.25.3 ± 0.2
Data are presented as mean ± SE. Sol background EMG (µV) (EMG 30–50 ms before test stimulus).
Table 2. Maximum amplitude values of Sol.
Table 2. Maximum amplitude values of Sol.
ShamIllusion
9.7 ± 0.59.5 ± 0.6
Data are presented as mean ± SE (mV).
Table 3. Amplitude values of M waves in the TA.
Table 3. Amplitude values of M waves in the TA.
PrePost 0Post 5Post 10
Sham66.8 ± 8.872.3 ± 8.568.7 ± 8.970.0 ± 8.4
Illusion67.9 ± 7.569.4 ± 7.170.6 ± 6.869.2 ± 7.3
Data are presented as mean ± SE (µV).
Table 4. Sol H-reflex amplitude (%Mmax).
Table 4. Sol H-reflex amplitude (%Mmax).
PrePost 0Post 5Post 10
ShamSingle19.6 ± 0.619.4 ± 0.319.2 ± 0.419.5 ± 0.5
CTI 2 ms17.1 ± 0.6 †18.2 ± 0.4 *17.6 ± 0.7 *18.5 ± 0.6
CTI 20 ms14.6 ± 0.8 †15.1 ± 0.6 †14.7 ± 0.5 †15.2 ± 0.5 †
IllusionSingle20.2 ± 0.520.1 ± 0.519.9 ± 0.520.2 ± 0.5
CTI 2 ms18.6 ± 0.7 *17.8 ± 0.9 **18.5 ± 0.8 *17.9 ± 1.0 **
CTI 20 ms15.9 ± 0.8 †14.8 ± 0.7 †16.3 ± 0.6 †14.3 ± 0.8 †
Data are presented as mean ± SE. Table 4 displays the results of each measurement over all intervention conditions. The value represents H-reflex/Mmax × 100. The data were analyzed by comparing the H-reflex amplitude value of the single condition divided by Mmax vs. the H-reflex amplitude value divided by Mmax for each of the two CTI conditions (2 and 20 ms). CTI, conditioning stimulation–test stimulation interval. * p < 0.05, ** p < 0.01, † p < 0.001.
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Okouchi, T.; Hirabayashi, R.; Sugai, N.; Yokota, H.; Sekine, C.; Ishigaki, T.; Komiya, M.; Sakamoto, K.; Edama, M. Impact of Visual Kinesthetic Illusions on Reciprocal Inhibition and Motor Function. Appl. Sci. 2024, 14, 11725. https://doi.org/10.3390/app142411725

AMA Style

Okouchi T, Hirabayashi R, Sugai N, Yokota H, Sekine C, Ishigaki T, Komiya M, Sakamoto K, Edama M. Impact of Visual Kinesthetic Illusions on Reciprocal Inhibition and Motor Function. Applied Sciences. 2024; 14(24):11725. https://doi.org/10.3390/app142411725

Chicago/Turabian Style

Okouchi, Takeru, Ryo Hirabayashi, Nao Sugai, Hirotake Yokota, Chie Sekine, Tomonobu Ishigaki, Makoto Komiya, Kodai Sakamoto, and Mutsuaki Edama. 2024. "Impact of Visual Kinesthetic Illusions on Reciprocal Inhibition and Motor Function" Applied Sciences 14, no. 24: 11725. https://doi.org/10.3390/app142411725

APA Style

Okouchi, T., Hirabayashi, R., Sugai, N., Yokota, H., Sekine, C., Ishigaki, T., Komiya, M., Sakamoto, K., & Edama, M. (2024). Impact of Visual Kinesthetic Illusions on Reciprocal Inhibition and Motor Function. Applied Sciences, 14(24), 11725. https://doi.org/10.3390/app142411725

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