|
 
 |
| ORIGINAL ARTICLE |
|
| Year : 2022 | Volume
: 39
| Issue : 2 | Page : 79-84 |
|
The effect of motor imagery on the excitability of spinal segmentary reflexes in restless legs syndrome patients
Figen Yavlal1, Meral Erdemir Kızıltan2
1 Department of Neurology, Medicana International Istanbul Hospital, Istanbul, Turkey
2 Department of Neurology, Cerrahpaşa School of Medicine, Istanbul University, Istanbul, Turkey
| Date of Submission | 13-Dec-2020 |
| Date of Decision | 01-May-2021 |
| Date of Acceptance | 04-Jul-2021 |
| Date of Web Publication | 29-Apr-2022 |
Correspondence Address:
Figen Yavlal
Medicana International Istanbul Hastanesi, Clinic of Neurology, Istanbul
Turkey
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/nsn.nsn_221_20
Context: Restless legs syndrome (RLS) is a neurological sleep disorder which causes an overwhelming urge to move the legs. However, this spinal excitability can be decreased through the use some motor movements such as walking or stretching. Aims: This study aimed to investigate the effect of motor imagery (MI) on spinal excitability in relation to the H reflex (HR). Settings and Design: In this study, 11 patients diagnosed with RLS (3 males and 8 females, mean age: 41.2) and 14 controls (8 males and 7 females, mean age: 38.4) were tested. HR was studied while participants in the supine position were imagining walking and also while imagining both dorsiflexion (DF) and plantar flexion (PF). Results: There was significant decrease in the Hmax/Mmax at 90° DF in both groups (p = 0.002, p = 0.001). There was no significant decrease in the RLS group on imagery; however, there was a significant decrease in the control group with movement imagination compared to the resting state (p = 0.021). There was no significant increase in Hmax/Mmax at 135° PF in both groups on movement and imagery. There was a decrease in the ratio on the imagery of walking in the RLS group (p = 0.038), but the same ratio increased in the control group (p = 0.010). Conclusion: As motor movements decrease corticospinal excitability in RLS, the imagery of movement mimicking the actmovement can relieve the symptoms of RLS. As a conclusion, further electrophysiological studies can be useful to gauge the effects of MI on spinal excitability in RLS.
Keywords: H reflex, motor imagery, restless legs syndrome, spinal excitability
How to cite this article:
Yavlal F, Kızıltan ME. The effect of motor imagery on the excitability of spinal segmentary reflexes in restless legs syndrome patients. Neurol Sci Neurophysiol 2022;39:79-84 |
How to cite this URL:
Yavlal F, Kızıltan ME. The effect of motor imagery on the excitability of spinal segmentary reflexes in restless legs syndrome patients. Neurol Sci Neurophysiol [serial online] 2022 [cited 2023 Mar 27];39:79-84. Available from: http://www.nsnjournal.org/text.asp?2022/39/2/79/345001 |
| Introduction | |  |
Restless legs syndrome (RLS) is a neurological sleep and movement disorder that causes an unstoppable urge to move the legs, and which is frequently accompanied by unpleasant sensations.[1] An increase in these urges is observed during evenings and nights due to the disorder's circadian character.
Studies have demonstrated an increase in excitability in the cortical motor pathways and indirectly at spinal level in RLS.[2],[3],[4] Intracortical facilitation (ICF) decreases when leg movements stimulate the cortical areas, by which the increase in excitability can be controlled through various motor movements such as walking or stretching.[5]
It has been suggested that there is a similarity between physically performing a movement and the neural processes that take place during motor imagery (MI) of such movement.[6] fMRI and positron emission tomography studies have identified a blood buildup in similar cortical structures during the actual movement and MI. As well, many transcranial magnetic stimulation (TMS) studies have accepted the existence of an increase in cortical and corticospinal pathway excitability during MI.[7] The imagery of walking is a complex area of MI. Walking is considered complex in that it is a combined movement consisting of simple movement stages such as the dorsiflexion (DF) and plantar flexion (PF) of the foot. The imagery of a simple movement prepares the corticospinal structures for a complex movement taking place using the same muscles and increases excitability.[8] It was demonstrated that the H reflex (HR) amplitude changes during the phases of actual walking and pacing. In spite of these data indicating an increase in excitability in respect to the cortical level, the results of HR studies, in which the spinal level was examined during MI is debatable, and HR studies conducted during walking imagery are limited in the literature.
While the actual movement or its imagery activate the same regions in the corticospinal pathway, not only the actual movement itself, but also its imagery is expected to reduce increased spinal excitability.
Setting out from these data, this research aimed at comparing the electrophysiological changes in the excitability of the motor system at the spinal level by conducting an HR examination during rest and MI in patients diagnosed with RLS.
| Subjects and Methods | | |
In this study, patients diagnosed with RLS at the Sleep Disorders Polyclinic were subjected to clinical and electrophysiological examination. Motor restlessness gradually increased during the day due to the circadian feature in the pathophysiology of RLS and reached a maximum in the hours following midnight, while no shift in other physiological rhythms was detected. Increasing of symptoms in RLS patients toward evening or night time has been determined as one of the diagnostic criteria of the disease by the International Restless Legs Syndrome Study Group (IHBSSG). For the current study, our patients were selected from the idiopathic RLS group in accordance with these criteria. Patients who received an RLS diagnosis for the first time, and for whom no treatment was initiated for RLS, were included in the study. The control group was chosen parallel to the RLS group in terms of age and gender. In both groups, patients having metal objects such as implants, pacemakers, bone plates, and those suffering from neurological (peripheric neuropathy and lumbar disc disease), psychiatric (depression, psychosis, and use of antidepressants-antipsychotics), or internal diseases (diabetes mellitus, thyroid dysfunction, and related medication use) were excluded from the study. The study was approved by the local ethics committee (No. 83045809/466 on January 16, 2014), and the participants who participated in the study signed an informed consent form.
Of the 25 participants included in the study, 11 were RLS patients and 14 were healthy volunteers compatible with the RLS group. [Table 1] provides demographic data on the RLS cases and the healthy control group. The ages and genders of the groups displayed a similar distribution.{Table 1}
Electrophysiological examination
The HR study for all participants in the study was performed between 13:30 and 15:00. A Neuropack Sigma MEB-5500 (Nihon Kohden, Tokyo, Japan) EMG device was used in these examinations. The examinations were conducted with the subjects in the supine position, while resting and after allowing the patients to relax.
Each stage of the examinations to be conducted was explained and instructions were given to the participants. For the walking imagination paradigm, participants were asked to imagine that they were walking on a level clearing at a tempo that was average for them, and to continue this, until they received the instruction to “stop.”
H reflex
Data were collected by placing the cathode of the stimulating electrode on the proximal and the anode on the distal, with the active electrode on the center of the soleus muscle and the reference electrode on the calcaneal tendon; the tibial nerve was stimulated by a single electric current of a duration of 0.5 ms at the popliteal fossa. In this position, first, the maximum muscle response (Mmax) was obtained, then the HR study proceeded. The stimuli were given at minimum intervals of 3–5 s in order to prevent habituation. The sweep speed was set at 10 ms, sensitivity at 0.5–5 mV, and the filters at 10–500 Hz. For the HR response observed following the first-received M response while increasing the value of the electrical stimulus, the characteristic of the H amplitude of dropping with an increase in the H amplitude was used for the recognition of the reflex. The strength of the current was increased by 0.5–1.0 mA until the maximum HR amplitude and the minimum motor response were obtained. Maximum HR amplitude was determined as interpeak (peak to peak). The maximum HR responses were recorded for the planned rest and imagery conditions. The maximum HR amplitude was divided by the amplitude of the maximum M response to obtain the Hmax/Mmax ratios. Two stages of examinations were conducted:
- At rest, while performing a 90° DF and 135° PF, and while imagining performing these movements
- An HR recording was taken, while the subjects were at rest and were imagining, they were walking on a level clearing at a tempo that was average for them, and a mean value was obtained by taking five reproducible recordings at each stage.
HR recordings were taken at rest, before, during, and after imagining, after the verbal description of the relevant movement, and while monitoring the relevant movement.
Statistics
The Pearson Chi-square test was used for the categorical variant in keeping with the gender, age, motor response latency according to the patient and control groups, motor response amplitude, HR latency, and HR amplitude levels. In the 90° DF and 135° PF Hmax/Mmax values, whether the group had an impact on the difference between the actual and imaginary movement averages was evaluated using independent samples t-tests for before, during, and after movement. The computations were performed using R-3.6.0 (for Windows. The R-project for statistical computing), The jamovi project (2018). jamovi (Version 0.9.5.12) [Computer Software]) Retrieved from https://www.jamovi.org and IBM SPSS Statistics (Version 24). The significance level was considered as 0.05 (P value) in the statistical analyses.
| Results | | |
A-Hmax/Mmax ratio at rest for restless legs syndrome and control groups
When the Hmax and Mmax values taken from the participants at the beginning of the study were compared, it was found that the mean Hmax/Mmax was 57.7% ±35.6 for healthy participants and 51.99% ±21.42 for the RLS group, and that there was no statistically significant difference between the two groups (p = 0.232).
B-the Hmax/Mmax ratio in the restless legs syndrome and control groups in the actual and imaginary 90° dorsiflexion movement
In both groups, the Hmax values at rest which were obtained before, during, and after the 90° DF movement demonstrated a marked drop followed by a rise in active movement compared to rest. When comparing these Hmax values to the Mmax values, it was found that the drop during active movement found in comparison to rest was statistically significant in both groups (p = 0.002 in the RLS group, p = 0.001 in the control group).
In the same manner, there was a drop in the Hmax/Mmax ratios in both groups compared to rest before the actual and imaginary 90° DF movement, but while the drop in the RLS group presented no statistically significant difference, the drop in the control group was statistically significant (p = 0.021) [Graph 1].[INLINE:1]
C-the Hmax/Mmax ratio for the restless legs syndrome and control groups in the actual and imaginary 135° plantar flexion dorsiflexion movement
In both groups, the Hmax values at rest obtained before, during, and after the 135° PF movement demonstrated a marked rise followed by a drop in active movement compared to rest. When comparing these Hmax values to the Mmax values, it was found that the rise during active movement found in comparison to rest was not statistically significant in both groups (p = 0.20 in the RLS group, p = 0.52 in the control group).
In the same manner, there was a rise in both groups in the Hmax/Mmax ratios before and during the imaginary 135° DF movement compared to rest, however the rise in both groups was not statistically significant (p = 0.18, p = 0.15) [Graph 2].[INLINE:2]
D-evaluation of the Hmax/Mmax ratio during the walking imagery for the restless legs syndrome and control groups
For the control group, on the other hand, the value obtained during the walking imagery having increased compared to the preimagery value was statistically significant (p = 0.010).
The fact that the Hmax/Mmax ratio obtained during the walking imagery for the RLS group dropped compared to the preimagery value was considered statistically significant (p = 0.038) [Graph 3].[INLINE:3]
| Discussion | | |
The main hypothesis was that just as motor movement relieves symptoms in RLS sufferers, MI would also relieve spinal excitability. While a statistically significant decrease was found in the Hmax/Mmax ratios recorded at 90° DF compared to rest in both groups, it was demonstrated that the downtrend continued also when the movement was imagined. In the measurements performed for the actual and imagined 135° PF movement, uptrend was observed in the Hmax/Mmax ratio for actual and imaginary movement in both groups. While the Hmax/Mmax ratios achieved in the HR study with imagined walking demonstrated a marked drop in the RLS group, an increase was identified in the control group. In order to evaluate the effect of MI in reducing increased excitability in the pathophysiology of RLS, the basis of this study, the obtained results were compared to the literature.[9],[10]
The contraction of the Tibialis Anterior muscle while performing DF while studying Soleus HR should normally have caused reciprocal inhibition, and an inhibition in the HR, that is, a reduction in HR amplitude should have been observed. At this phase of the test, the drop in amplitude expected in both groups was observed. It is possible to also construe this situation as the absence of a reciprocal inhibition disorder in the RLS group, albeit a rough one. The fact that there was a drop in the mean values recorded for both groups during the imagery of the simple DF movement compared to rest, and the subsequent increase following movement or its imagery, reflect changes in corticospinal excitability. Similarly, Aoyama and Kaneko, in which DF and PF imagery were similarly studied, were not compatible with the findings of the present research since they had failed to find change in HR in both cases.[11]
In the literature, spinal excitability changes in MI performed with HR yielded different results. This incompatibility was researched by combining HR and F-wave techniques on MI with TMS. Certain researchers failed to observe changes in the HR amplitude obtained from the Extensor Carpi Radialis[12] and Flexor Digitorum Superficialis[13] muscles through MI. These results demonstrate that MI was effective in an increase in spinal transmission, and when comparing rest with MI, caused an increase in plantar flexor HR amplitude.[14] It was found that this increase was proportional to the intensity of the imagined contraction.[15]
The reasons for the different HR results obtained in the present study are (1) presynaptic inhibition in the Ia fibers, (2) the change in Ia neurotransmitter release amounts, and (3) changes in motor neuron excitability varying in accordance with excitatory and inhibitory inputs.[16] The suprasegmental mechanism affecting HR amplitude during MI is not independent of these factors. The higher Hmax values recorded in actual and imaginary 135° PF in the RLS and control groups in these results when compared to rest represent the reciprocal inhibition of Ia interneurons.[17],[18],[19] While the brain sends the command to contract to the extensor muscle during imagined extension, the antagonistic flexor muscle motor neuron is inhibited by Ia interneurons. In light of the data in the literature,[18],[19] it was considered that PF was not suitable for actual and imagined movement for such a test.
As suggested by Jeannerod, MI means unperformed movement in spite of the activation of the primary motor cortical areas.[20] This phenomenon may be explained through two theories: (1) the existence of a mechanism performing an inhibitory block on the motor command initiated by the motor cortex[21] and/or (2) cortical activation during MI proves too weak to create a muscle response, while nevertheless succeeding in reaching a subordinate nerve level.[22],[23] When comparing the values obtained from actual movement with those recorded during imagery, the values obtained during imagery were found to be not as distinct as those obtained during actual movement, although they were in the same direction. This indicates that the command for the imagined movement is too weak for cortical activation but is capable of adequately reaching spinal level.[24] Several authors comparing EMG muscle responses at rest through MI believed that the reason for the different results obtained in actual movement could be attributed to individual differences in intensity for the contraction of the imagined movement. While some found the obtained responses to be proportional with the level of the imagination,[25] others found no motor activity in the EMG.[26] These results demonstrate that, although the corticospinal excitability level during MI is lower compared to the level emerging as a result of actual movement, the modulation of the activation is similar in both cases in terms of quality.
Again, the absence of HR change in the case of MI should suggest activation in spinal interneurons, which have a low stimulation threshold.[27] It may be considered that the increase in Hmax following MI for a movement for which excitation is expected during actual movement could be an outcome of a decrease in spinal presynaptic inhibition rather than representing a direct effect on alpha motor neuron output. Conversely, it may be assumed that the inhibition in question increases when imagining a movement, for which inhibition is expected.[28]
It has been reported that the MI of walking increased the MEPs in lower extremity muscles.[29] It is known that spinal reflex excitability is modulated during walking in a phase-dependent manner. For instance, the H reflex amplitudes during walking are greater in the halting phase compared to the release phase.[30] The modulation dependent on this phase is generated by both somatosensorial inputs and more cortical inputs during walking. Using the passive movement paradigm, the effects of somatosensorial inputs on H reflex during walking were studied.[31]
The image of walking is a complex area of MI. Walking is a complex combined movement consisting of simple movement stages such as the DF and PF of the foot. The imagining of a simple movement prepares the corticospinal structures for a complex movement taking place using the same muscles and increases excitability.[8] The most striking outcome of this study was that the Hmax/Mmax values which emerged during the imagining of walking demonstrated a drop in the RLS group and a rise in the control group when compared to preimagining values. The decrease of spinal excitability increased in the RLS group with the imagining of walking was parallel to the decrease in spinal excitability caused by actual movement, thereby conforming to daily living practice.
It is understood that cortical preparation is more complex in the imagery of walking compared to that, in simple movements, while also affecting the excitability of the spinal motor neuron pool. The increase in spinal excitability with the imagining of walking in the control group within this study strengthens this theory. In the RLS group, on the other hand, HR excitability decreased during MI.
Functional anatomy studies found confusion in the supraspinal inhibitory system and[32] a disorder in the regulation of the spinal cord cycle in[4] RLS patients, which suggests that RLS may be caused by dysfunction in the dopaminergic neurons of the basal ganglia effecting a change on sensorimotor activity in the spinal cord. It is known that an effort is made to reduce the corticospinal excitability that increases in RLS through leg movements. Studies have demonstrated findings relating to cortical retention in RLS,[5] indicating that leg muscles decrease ICF by stimulating cortical areas.
In the light of these findings and discussion, the conclusion of this research is that MI affects spinal excitability, and walking imagery causes a decrease in H reflex excitability. While walking or performing another motor movement can decrease corticospinal excitability that increases in RLS, it may be possible to achieve a similar result through MI
Limitations
While the nighttime excitability decreases in normal individuals, there is no decrease in RLS and RLS symptoms increase in the evening or at night. Since we performed our electrophysiological examination during the daytime, the patients were not questioned for symptoms during and after the examination. H reflex responses were evaluated during rest and MI, as the basis of the study was to determine the changes in excitability during MI.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Maung SC, El Sara A, Chapman C, Cohen D, Cukor D. Sleep disorders and chronic kidney disease. World J Nephrol 2016;5:224-32.  |
| 2. | Winkelmann J, Trenkwalder C. Pathophysiology of restless-legs syndrome. Review of current research. Nervenarzt 2001;72:100-7. |
| 3. | Zucconi M, Manconi M, Ferini Strambi L. Aetiopathogenesis of restless legs syndrome. Neurol Sci 2007;28 Suppl 1:S47-52. |
| 4. | Rijsman RM, Stam CJ, de Weerd AW. Abnormal H-reflexes in periodic limb movement disorder; impact on understanding the pathophysiology of the disorder. Clin Neurophysiol 2005;116:204-10. |
| 5. | Paulus W, Dowling P, Rijsman R, Stiasny-Kolster K, Trenkwalder C. Update of the pathophysiology of the restless-legs-syndrome. Mov Disord 2007;22 Suppl 18:S431-9. |
| 6. | Chen X, Wan L, Qin W, Zheng W, Qi Z, Chen N, et al. Functional preservation and reorganization of brain during motor imagery in patients with incomplete spinal cord injury: A pilot fMRI study. Front Hum Neurosci 2016;10:46. |
| 7. | Stinear CM, Byblow WD. Modulation of corticospinal excitability and intracortical inhibition during motor imagery is task-dependent. Exp Brain Res 2004;157:351-8. |
| 8. | Bakker M, De Lange FP, Helmich RC, Scheeringa R, Bloem BR, Toni I. Cerebral correlates of motor imagery of normal and precision gait. Neuroimage 2008;41:998-1010. |
| 9. | Kasai T, Kawai S, Kawanishi M, Yahagi S. Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery. Brain Res 1997;744:147-50. |
| 10. | Facchini S, Muellbache W, Battaglia F, Boroojerdi B, Hallett M. Focal enhancement of motor cortex excitability during motor imagery: A transcranial magnetic stimulation study. Acta Neurol Scand 2002;105:146-51. |
| 11. | Aoyama T, Kaneko F. The effect of motor imagery on gain modulation of the spinal reflex. Brain Res 2011;1372:41-8. |
| 12. | Hashimoto R, Rothwell JC. Dynamic changes in corticospinal excitability during motor imagery. Exp Brain Res 1999;125:75-81. |
| 13. | Abbruzzese G, Trompetto C, Schieppati M. The excitability of the human motor cortex increases during execution and mental imagination of sequential but not repetitive finger movements. Exp Brain Res 1996;111:465-72. |
| 14. | Bonnet M, Decety J, Jeannerod M, Requin J. Mental simulation of an action modulates the excitability of spinal reflex pathways in man. Brain Res Cogn Brain Res 1997;5:221-8. |
| 15. | Jarjees M, Vuckovic A. The effect of voluntary modulation of the sensory-motor rhythm during different mental tasks on H reflex. Int J Psychophysiol 2016;106:65-76. |
| 16. | Clark S, Tremblay F, Ste-Marie D. Differential modulation of corticospinal excitability during observation, mental imagery and imitation of hand actions. Neuropsychologia 2004;42:105-12. |
| 17. | Knikou M. The H-reflex as a probe: Pathways and pitfalls. J Neurosci Methods 2008;171:1-12. |
| 18. | Yamaguchi T, Fujiwara T, Saito K, Tanabe S, Muraoka Y, Otaka Y, et al. The effect of active pedaling combined with electrical stimulation on spinal reciprocal inhibition. J Electromyogr Kinesiol 2013;23:190-4. |
| 19. | Yamaguchi T, Fujiwara T, Tsai YA, Tang SC, Kawakami M, Mizuno K, et al. The effects of anodal transcranial direct current stimulation and patterned electrical stimulation on spinal inhibitory interneurons and motor function in patients with spinal cord injury. Exp Brain Res 2016;234:1469-78. |
| 20. | Jeannerod M. Neural simulation of action: A unifying mechanism for motor cognition. Neuroimage 2001;14:S103-9. |
| 21. | Guillot A, Hoyek N, Louis M, Collet C. Understanding the timing of motor imagery: Recent findings and future directions. Int Rev Sport Exerc Psychol 2012;5:3-22. |
| 22. | Lebon F, Collet C, Guillot A. Benefits of motor imagery training on muscle strength. J Strength Cond Res 2010;24:1680-7. |
| 23. | Lebon F, Rouffet D, Collet C, Guillot A. Modulation of EMG power spectrum frequency during motor imagery. Neurosci Lett 2008;435:181-5. |
| 24. | Wright DJ, Williams J, Holmes PS. Combined action observation and imagery facilitates corticospinal excitability. Front Hum Neurosci 2014;8:951. |
| 25. | Guillot A, Collet C. Contribution from neurophysiological and psychological methods to the study of motor imagery. Brain Res Brain Res Rev 2005;50:387-97. |
| 26. | Gentili R, Papaxanthis C, Pozzo T. Improvement and generalization of arm motor performance through motor imagery practice. Neuroscience 2006;137:761-72. |
| 27. | Grosprêtre S, Lebon F, Papaxanthis C, Martin A. New evidence of corticospinal network modulation induced by motor imagery. J Neurophysiol 2016;115:1279-88. |
| 28. | Ruffino C, Papaxanthis C, Lebon F. Neural plasticity during motor learning with motor imagery practice: Review and perspectives. Neuroscience 2017;341:61-78. |
| 29. | Kaneko N, Masugi Y, Yokoyama H, Nakazawa K. Difference in phase modulation of corticospinal excitability during the observation of the action of walking, with and without motor imagery. Neuroreport 2018;29:169-73. |
| 30. | Nakagawa K, Masugi Y, Saito A, Obata H, Nakazawa K. Influence of motor imagery on spinal reflex excitability of multiple muscles. Neurosci Lett 2018;668:55-9. |
| 31. | Masugi Y, Kitamura T, Kamibayashi K, Ogawa T, Ogata T, Kawashima N, et al. Velocity-dependent suppression of the soleus H-reflex during robot-assisted passive stepping. Neurosci Lett 2015;584:337-41. |
| 32. | Entezari-Taher M, Singleton JR, Jones CR, Meekins G, Petajan JH, Smith AG. Changes in excitability of motor cortical circuitry in primary restless legs syndrome. Neurology 1999;53:1201-5. |
|
Search Pubmed for