Is Reciprocal Facilitation a Myth in Upper Motor Neuron Lesions?

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Eser Kalaoglu, Mustafa Kokce, Mert Çetin, Kemal Türker, Ilhan Karacan This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4178539/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Study Design: Clinical trial Objective: To investigate whether reciprocal facilitation is a pseudo-reflex response resulting from crosstalk or cross-stimulation using the MMU EMG technique. Setting: Istanbul Physical Therapy Rehabilitation Training and Research Hospital, Istanbul, Turkiye Methods: Five individuals with chronic incomplete spinal cord lesions (SCL) and five able-bodied volunteers participated in the study. To trigger the reciprocal facilitation response in the tibialis anterior muscle, the Soleus T-reflex was induced by tapping the Achilles tendon, while the Soleus H-reflex was elicited by stimulating the tibialis nerve. Reflex responses were simultaneously recorded from the right soleus and right tibialis anterior muscles using both surface electromyography (sEMG) and multi-motor unit (MMU) EMG. Results: It was noted that the EMG responses initially interpreted as reciprocal facilitation in both able-bodied individuals and those with SCL were actually due to cross-stimulation. Specifically, it was found that when the tibial nerve was stimulated with an electrical current to evoke the soleus H-reflex, simultaneous stimulation of the peroneal nerve occurred, resulting in the occurrence of both tibialis anterior H-reflex and M wave (cross-electrical stimulation). Additionally, striking the Achilles tendon with a reflex hammer to elicit the soleus T-reflex resulted in mechanical stimulation spreading to both the soleus and tibialis anterior muscle bellies, activating the muscle spindles and eliciting both soleus and tibialis anterior T-reflex responses (cross-mechanical stimulation). Conclusions: No evidence supporting reciprocal facilitation was found. Further research utilizing H-reflex and T-reflex tests, resolving the cross-stimulation issue, is needed to establish its existence conclusively. Health sciences/Neurology/Neurological disorders/Movement disorders Biological sciences/Neuroscience/Motor control spinal cord injury paraplegia tetraplegia reciprocal inhibition Figures Figure 1 Figure 2 Figure 3 1. Introduction Sherrington described reciprocal innervation as the spinal mechanism regulating the movements of agonist and antagonist muscle groups. It involves the activation of an agonist motor neuron pool, which leads to the inhibition of the corresponding antagonist motor neuron pool. This process ensures that while agonists contract, antagonists relax, allowing coordinated movement [ 1 ]. Reciprocal (antagonist) inhibition involves a disynaptic circuit in the spinal cord, influenced by various supraspinal and segmental modulatory mechanisms [ 2 ]. Additionally, presynaptic inhibition and other neural mechanisms have been proposed to contribute to antagonist inhibition [ 3 , 4 ]. Disruptions in antagonist inhibition are a notable characteristic of human spasticity, wherein involuntary co-contractions of antagonist muscles frequently occur instead of selective activation of agonists [ 5 , 6 ]. The occurrence of co-contraction in the spastic limb is attributed to the disappearance of antagonist inhibition and the emergence of reciprocal facilitation in its place [ 7 , 8 , 9 , 10 ]. However, convincing evidence supporting this hypothesis is currently lacking. Reciprocal Ia inhibition can either increase, decrease, or disappear entirely, depending on various factors such as the underlying cause of the disease, the location of the lesion, the severity of spasticity, and the extent of functional recovery [ 10 ]. While antagonist inhibition/facilitation is straightforward, identifying reciprocal inhibition/facilitation poses more challenges. There are some electrophysiological studies, however, that support reciprocal facilitation where reflex responses were captured using surface EMG (sEMG) [ 7 , 8 , 10 ]. Nonetheless, a notable limitation of sEMG is the potential for crosstalk In sEMG, signals from agonist reflex muscles may inadvertently be recorded by antagonist muscle electrodes, giving a false impression that the reflex responses are coming from the antagonist muscle. Multi-motor unit (MMU) EMG is widely recognized as reliable for identifying crosstalk as it records action potentials of active motor units from a small portion of the muscle of interest [ 11 ]. Using the MMU EMG technique, this study tests whether reciprocal facilitation is an erroneous interpretation resulting from crosstalk. Establishing the validity of electrophysiological evidence indicating the emergence of the reciprocal facilitation phenomenon in upper motor neuron lesions is crucial. Specific anti-spastic treatment methods, like cold therapy and proprioceptive neuromuscular stimulation, use the concept of antagonist inhibition [ 12 , 13 , 14 ]. However, suppose reciprocal facilitation proves to be a valid phenomenon. In that case, it will significantly impact the development of new treatment methods for patients suffering from upper motor neuron lesions. 2. Methods 2.1. Participants In this quasi-experimental study, five individuals with chronic incomplete spinal cord lesions (SCL) participated, with an average age of 46.8 years (± 16.5), comprising 4 females and 1 male. Additionally, five able-bodied volunteers took part, with an average age of 28.6 years (± 3.3), including 3 females and 2 males. Patients with premorbid neuromuscular disease or a history of autonomic dysreflexia were not included in the study. All participants provided informed consent prior to participation. All experimental procedures were designed with the Helsinki Declaration in mind and were approved by the local ethics committee (Approval Number: 2022-17-19). The study protocol was registered with ClinicalTrials.gov (NCT05985031). The average duration of spinal cord injury was 9.4 years, ranging from 5 to 15 years. All individuals with SCL were classified as paraplegic. Among them, four had traumatic SCL and one had a non-traumatic SCL. Two were classified as AIS (ASIA (American Spinal Injury Association) Impairment Scale) C class, and three were classified as AIS D class. Using the modified Ashworth scale, soleus spasticity was rated as score 1 in one case, 1 + in three cases, and score 2 in one case. 2.2. Procedures In the present study, to evoke the tibialis anterior muscle reciprocal facilitation response, the Soleus T-reflex was elicited by tapping the Achilles tendon, while the Soleus H-reflex was elicited by stimulating the tibialis nerve. Participants were positioned safely and comfortably in a prone position on the examination table. Reflex responses were recorded simultaneously from the right soleus and right tibialis anterior muscles using both sEMG and MMU EMG. 2.2.1. Eliciting the soleus reflex response To elicit the soleus T-reflex, fifteen consecutive strokes of constant intensity were applied to the right Achilles tendon with the ankle in a neutral position. To prevent the development of depression after homosynaptic activation in patients with upper motor neuron lesions, it is recommended to maintain a minimum interval of 10 seconds between successive stimulations [ 15 ]. In this study, the time between tendon strokes was kept longer than 10 seconds. To elicit the soleus H-reflex, the right tibial nerve was stimulated using a monopolar technique with a square-shaped monophasic electric current featuring a pulse duration of 1 ms. The anode, sized 10x10 cm, was positioned on the suprapatellar region, while the cathode electrode, with a diameter of 1 cm and hemispherical in shape, was placed on the tibial nerve at the midpoint of the fold line in the popliteal fossa. Electrocardiography (ECG) gel was applied beneath the electrodes to enhance conductivity, and the electrodes were securely affixed to the skin. The rest period between successive electrical stimulations was at least 10 seconds. Electrical stimulations were administered using a constant current generator (model DS7A, Digitimer Ltd, Hertfordshire, UK). A recruitment curve was generated for each participant by gradually increasing the stimulus intensity. This process identified the current intensities corresponding to the onset of the H-reflex (Hmin), the minimum M-response (Mmin), and the disappearance of the H-reflex alongside the attainment of the maximum M-response (Mmax). The range of current intensity that elicited the Hmin and Mmax responses from the right tibial nerve was divided into ten equal increments. At each intensity level, the right tibial nerve underwent stimulation via the popliteal fossa five times. Simultaneously, monitoring was conducted to identify any instances of reciprocal facilitation in the Tibialis anterior muscle sEMG and MMU EMG recordings. 2.2.2. Data recording A pair of self-adhesive Ag/AgCl (Redline®) electrodes were applied to the skin following the SENIAM protocol to obtain superficial EMG recordings from the right soleus and tibialis anterior muscles using the bipolar technique [ 16 ]. The ground electrode was affixed to the right lateral malleolus. Before applying the electrodes, any hair on the skin was shaved, the skin was lightly abraded to remove dead skin using sandpaper, and the skin surface was cleaned with alcohol wipes to remove any oil residue. ECG gel was then applied to the skin area beneath the electrodes to increase skin moisture, ensuring skin resistance between the electrodes remained below 10 kOhm. To record soleus and tibialis anterior EMG signals using MMU EMG, a pair of silver wire electrodes (75 µm core diameter) insulated with Teflon, except for the cut ends, was utilized. These wires were threaded through the channel of a 25 G needle, and their ends were shaped like fishhooks, with a distance of approximately 3 mm between them. The pair of wires was inserted between two surface EMG electrodes into the muscle to a depth of about 3 cm, using the needle. The needle was then removed, leaving the fishhooked wires inside the muscle. A lip-clip electrode served as the ground electrode [ 17 , 18 ]. An accelerometer (LIS344ALH, ± 6 g full-scale range, linear accelerometer, ECOPACK®, Mansfield, TX, USA) was employed to measure the latency of the Achilles tendon reflex. All EMG and accelerometer recordings were obtained using a data recorder (CED 1902 Quad System MKIII amplifier and CED 3601 Power 1401 MKII digital-to-analog converter, Cambridge Electronic Design Limited, Cambridge, England) and analyzed using software (Cambridge Electronic Designs Spike2®). The sampling rate for recordings was set at 2 kHz for sEMG and accelerometer data, and 10 kHz for MMU EMG recordings. 2.2.3.Data Analysis Detection of reciprocal facilitation All EMG and accelerometer recordings underwent processing with infinite impulse response filters (Butterworth, 2nd order). The sEMG recordings were filtered using a 20–500 Hz band-pass filter, while the intramuscular recordings were filtered using a 100–5000 Hz band-pass filter. Spike-triggered averaging was conducted using the onset point as the trigger and the electrical signals recorded by EMG electrodes as the source to assess reciprocal facilitation. This procedure entailed averaging 5 ms of filtered EMG data before the trigger and 50 ms after it. Extraction of motion artifact signals The onset point of the tap-induced mechanical stimulus was visually marked on the accelerometer recording. This onset point served as the trigger for spike-triggered averaging, using the electrical signals recorded by MMU electrodes as the source. Spike-triggered averaging aimed to extract motion artifact signals from the total background tension generated by the asynchronous firing of active synergist motor units. The exact onset of the mechanical artifact in the averaged EMG recordings was determined using the CUSUM method [ 19 ]. Measurement of T- reflex latency An accelerometer was affixed to the Achilles tendon to assess the timing and intensity of tendon tapping with the reflex hammer. The raw reflex latency was determined as the period between the onset of impact on the tendon, detected by the accelerometer, and the onset of the T-reflex in the sEMG recordings. These measurements were adjusted for the delay of the mechanical artifact, identified using MMU electrodes. The duration for mechanical stimulation to reach the soleus and tibialis anterior muscle belly was determined, subtracted from the raw T-reflex latencies, and reported as T-reflex latency in the Results section. 2.2.4.Outcome measures The primary outcome measures of this study include the H-reflex, M-wave, and T-reflex. The secondary outcome measure was the mechanical artifact induced by the reflex hammer during the tap on the Achilles tendon. The interpretations of the H-reflex and M-response findings in both muscle sEMG and MMU-EMG recordings are as follows: reciprocal facilitation, cross-talk, or direct stimulation of the peroneal nerve (Cross-electrical stimulation) (Table 1 ). Table 1 The interpretations of the findings of H-reflex studies Scenarios Soleus sEMG / MMU EMG Tibialis anterior Interpretation sEMG MMU EMG Scenario − 1 H-reflex (+) H-reflex (+) H-reflex (+) Reciprocal facilitation M-wave (+) M-wave (-) M-wave (-) Scenario − 2 H-reflex (+) H-reflex (+) H-reflex (-) Cross-talk M-wave (+) M-wave (+) M-wave (-) Scenario − 3 H-reflex (+) H-reflex (+) H-reflex (+) Cross-stimulation M-wave (+) M-wave (+) M-wave (+) sEMG: Surface EMG, MMU: multi-motor unit The interpretations of the T-reflex in both muscle sEMG and MMU-EMG recordings are as follows: reciprocal facilitation, cross-talk, or tibialis anterior muscle spindle stimulation (cross-mechanical stimulation)(Table 2 ). Table 2 The interpretations of the findings of Achilles tendon T-reflex studies Scenarios TA T-reflex Mechanical artifact Timing the TA T-reflex Interpretation sEMG MMU Scenario − 1 (+) (+) - After soleus T-reflex Reciprocal facilitation Scenario − 2 (+) (-) - After soleus T-reflex Cross-talk Scenario − 3 (+) (+) + After/before soleus T-reflex cross-stimulation sEMG: Surface EMG, MMU: multi-motor unit 2.3.Statistical Analysis The normality of the data was assessed using the Shapiro-Wilk test. Continuous variables were presented as mean and standard deviation, while categorical variables were expressed as frequencies. Group means were compared using the Mann-Whitney U test. The Fisher exact probability test was employed to analyze the distribution of categorical variables among groups. The statistical significance was set at p < 0.05. The software package used for data management was PASW Statistics for Windows, Version 18.0 [SPSS Inc, Armonk, NY]. 2. Results In all individuals with SCL and all healthy controls, stimulation of the tibial nerve elicited an M wave with an H reflex in the tibialis anterior muscle; this suggests simultaneous direct stimulation of the peroneal nerve as well as the tibial nerve (Table 3 , Fig. 1 , 2 ). Table 3 indicates that in individuals with SCL, the tibialis anterior H-reflex appeared on average 0.5 ms before the Soleus H-reflex, while in the Control group, the tibialis anterior H-reflex appeared on average 1.5 ms before the Soleus H-reflex. Table 3 H-reflex studies findings in sEMG and MMU EMG Group Subject TA H-reflex TA M-wave H-reflex latency (ms) sEMG MMU sEMG MMU Tibialis anterior Soleus Difference SCL 1 + + + + 30.75 31.64 -0.89 2 + + + + 24.55 24.98 -0.43 3 + + + + 29.71 30.84 -1.13 4 + + + + 30.11 30.25 -0.14 5 + + + + 31.80 31.69 0.11 Control 1 + + + + 31.17 31.84 -0.67 2 + + + + 28.05 29.53 -1.48 3 + + + + 27.62 28.68 -1.06 4 + + + + 28.40 30.66 -2.26 5 + + + + 27.04 29.16 -2.12 TA: Tibialis anterior, sEMG: surface EMG, MMU: multi-motor unit When the Achilles tendon was struck with a reflex hammer, T-reflex responses occurred along with mechanical stimulation artifacts in both the soleus and tibialis anterior muscles in all cases (Table 4 , Fig. 3 ). The mechanical artifact reached the tibialis anterior MMU electrodes approximately 0.6 ms later in the SCL group and 0.9 ms later in the Control group compared to the soleus MMU electrodes. The T-reflex latency calculated based on the artifact was found to be 1.2 ms shorter in the SCL group and 2.2 ms shorter in the Control group compared to the soleus muscle in the tibialis anterior muscle (Table 4 ). Table 4 Findings of T-reflex studies in sEMG and MMU EMG and artifact in MMU EMG Group Subject TA T-reflex Artifact latency (ms) Reflex latency (ms) sEMG MMU TA artifact Soleus artifact TA T-reflex Soleus T- reflex Difference SCL 1 + NA 1.83 1.07 35.23 37.49 -2.26 2 + + 2.21 2.63 25.08 26.34 -1.26 3 + + 2.46 1.70 32.69 34.33 -1.65 4 + + 3.23 1.96 34.67 35.26 -0.59 5 + + 2.94 2.15 32.71 32.99 -0.27 Control 1 + + 3.12 2.29 34.16 35.00 -0.83 2 + + 1.88 1.39 31.81 33.10 -1.29 3 + + 4.91 3.27 28.39 32.34 -3.95 4 + + 2.84 1.57 31.54 35.54 -4.01 5 + + 1.92 1.51 31.08 31.89 -0.81 TA: Tibialis anterior 3. Discussion Unlike previous studies that examined the presence of reciprocal facilitation, this study, which included MMU EMG recordings in addition to sEMG, revealed two original findings: First, during the H-reflex study, the electrical current applied to stimulate the tibial nerve in the popliteal fossa also inadvertently stimulates the peroneal nerve nearby, a phenomenon termed cross-stimulation. Second, in the T-reflex study, when the Achilles tendon is tapped with a reflex hammer to elicit the soleus T-reflex, the resulting mechanical stimulation spreads to the belly of the tibialis anterior muscle, activating the muscle spindles and eliciting the tibialis anterior T-reflex response. Ultimately, no evidence supporting reciprocal facilitation was found. Methodological Considerations Xia and Rymer examined changes in the antagonist inhibition patterns between agonist and antagonist muscles of the ankle in individuals with complete SCL and incomplete SCL [ 8 ]. Their study, which included eight participants in each group, investigated these pattern changes under four specific conditions. These conditions involved applying a reflex hammer to either the tibialis anterior tendon or the Achilles tendon while the ankle was in full dorsiflexion or full plantar flexion. As a result, it has been reported that the reciprocal facilitation pattern is most frequently observed in cases with incomplete SCL by tapping the Achilles tendon during foot dorsiflexion (reciprocal facilitation in six out of eight cases in their study). Therefore, in this study, reciprocal facilitation was tested by performing an Achilles tendon hit in individuals with incomplete SCL. Unlike previous electrophysiological studies [ 8 , 20 , 21 ], this study involved both T-reflex and H-reflex tests, rather than focusing solely on the T-reflex or H-reflex alone. Given that the primary objective of this study was to discern whether reciprocal facilitation stemmed from cross-talk, a departure from prior research was made by incorporating MMU EMG electrode recordings alongside sEMG recordings. Cross-talk, a significant source of error, arises from electrical signals originating from adjacent muscles. Compared to sEMG, the MMU EMG technique boasts a superior signal-to-noise ratio, capturing signals from highly localized muscle areas. Consequently, MMU EMG serves as an effective safeguard against electrical signals (cross-talk) emanating from neighboring muscles [ 11 , 17 , 18 ]. Tests were also conducted on able-bodied volunteers to make comparisons in terms of cross-talk. Reciprocal facilitation vs Cross-talk or Cross-stimulation The inspiration for this research stemmed from Xia and Rymer's article [ 8 ], where they discussed the potential for cross-talk issues. However, it appears that no specific precautions were implemented in their research methodology to address this concern. In contrast, the present study utilized the MMU-EMG recording technique, which effectively discerns whether cross-talk is occurring [ 11 , 17 , 18 ]. Indeed, this study revealed that the primary concern is not cross-talk but rather cross-mechanical stimulation. In their study, Topkara et al. demonstrated that mechanical stimulation applied to the calcaneus extended not only to the soleus muscle but also to the quadriceps muscle, and this mechanical artifact was detectable using MMU electrodes [ 22 ]. When the Achilles tendon is struck with a reflex hammer, the resulting mechanical vibrations propagate through the soleus muscle, stimulating the muscle spindles and triggering the soleus T-reflex response. Moreover, in the present study, MMU EMG recordings revealed that mechanical stimuli also spread to the tibialis anterior muscle belly upon striking the Achilles tendon with a reflex hammer. It was determined that mechanical stimuli reached the tibialis anterior MMU electrodes within a time frame varying between 1.88–4.91 ms, and the soleus MMU electrodes within a time frame varying between 1.07–3.27 ms. If it had been observed that the TA T-reflex response occurred before the soleus T-reflex response when the Achilles tendon was struck, it would have been strong evidence for the view that the mechanical artifact stimulated the TA muscle spindles and triggered the T-reflex. However, the fact that the mechanical stimulus reaches the tibialis anterior muscle later than the soleus muscle and that the tibialis anterior T-reflex latency is shorter than the soleus T-reflex latency creates a complex picture that makes interpretation difficult. In controlled studies by Okuma et al. on five incomplete SCL patients and by Crone et al. on 11 SCL patients and six hemiplegic patients, it was reported that a reciprocal facilitation response occurred in the tibialis anterior muscle with tibial nerve stimulation [ 20 , 21 ]. In both studies, the tibial nerve was stimulated using the monopolar technique, similar to the method employed in the current study. Here, recordings were conducted using MMU electrodes, revealing that when the tibial nerve was stimulated with the monopolar technique, the peroneal nerve was simultaneously and directly stimulated (cross-stimulation phenomenon). The presence of an M response in MMU-EMG recordings, in addition to sEMG recordings, during tibial nerve stimulation serves as definitive evidence against the occurrence of cross-talk or reciprocal facilitation. If a reciprocal stimulation response had indeed occurred, only an H-reflex-like EMG response would have been observed without an M response. Conversely, in the case of cross-talk, M-wave and H-reflex responses would be observed in sEMG recordings, but not in MMU-EMG recordings. Limitation The number of individuals with incomplete SCL in this study may be considered small. As mentioned above, the frequency of antagonist inhibition among individuals with incomplete SCL was reported as 6/8 in the study by Xia and Rymer [ 8 ]. However, it's important to note that our study is not focused on the prevalence and clinical features of reciprocal facilitation; rather, it aims to assess the reliability of neurophysiological methods used to demonstrate its presence. Conclusion This study concluded that there were no findings supporting reciprocal facilitation. In H-reflex studies, it was shown for the first time that during stimulation of the tibial nerve with electrical current, the peroneal nerve was also stimulated (cross-electrical stimulation). In T-reflex studies, it has been demonstrated that when the tendon of the agonist muscle is struck, the antagonist muscle, as well as the agonist muscle, can be stimulated (cross-mechanical stimulation). However, due to the significant limitations (i.e., cross-stimulation) observed in H-reflex and T-reflex-based reciprocal facilitation tests, this study did not provide evidence supporting the existence of reciprocal facilitation in patients with SCL. Nevertheless, the findings of this study do not completely rule out the phenomenon of reciprocal facilitation in patients with upper motor neuron disease. Electrophysiological studies that provide solutions to the cross-stimulation problem are needed to definitively reveal the development of the reciprocal facilitation phenomenon in patients with upper motor lesions. Antagonist inhibition is the mainstay of approaches such as anti-spastic treatment with proprioceptive neuromuscular stimulation, ice applied to the antagonist muscle, and neuromuscular electrical stimulation in patients with upper motor neuron lesions [ 12 , 13 , 14 ]. Hence, it is crucial to elucidate the transition from antagonist inhibition to reciprocal facilitation in this context. Declarations COMPETING INTERESTS The authors declare no competing interests. References Sherrington CS. The Integrative Action of the Nervous System. Yale University Press, New Haven. 1906. Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol. 1992; 38:335–378. El-Tohamy A, Sedgwick EM. Spinal inhibition in man: depression of the soleus H reflex by stimulation of the nerve to the antagonist muscle. J Physiol. 1983; 337:497–508. Fu TC, Hultborn H, Larsson R, Lundberg A. Reciprocal inhibition during the tonic stretch reflex in the decerebrate cat. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4178539","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":288414015,"identity":"5d1a2397-d734-4354-9078-77f51267e203","order_by":0,"name":"Eser Kalaoglu","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABAElEQVRIiWNgGAWjYJACxgYGCyDF3MDwsQHMbzxAhBYJMMU4E8xibCBeCzMvhMWAVws//+FjH2fUSMjz8y9sk7bdYVOn234YaEuNTTQuLZIz0pJnbjgmYThzxsM26dwzaRJmZxKBWo6l5Tbg0GJwg8eY8QGbBOOGGweBWtoOS5gdAGphbDiMU4v9+fOfGR/8k7AHa7EEaTn/EL8WA4YcZsaNbRKJG843tkkzgrTcIGCLxI00Y8aZfRLJM2cwNlv2tqVJbrsBtCUBj1/4+w8/Zuz5ZmPbz3/44I2fbTb8ZufTHz74UGODUwuSfQlInAQcitDsO0CUslEwCkbBKBiBAADp/mTPhx+WnwAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0000-0001-8959-6522","institution":"Istanbul Physical Therapy Rehabilitation Training and Research Hospital","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Eser","middleName":"","lastName":"Kalaoglu","suffix":""},{"id":288414016,"identity":"3459b149-0062-4db7-b61e-581658160987","order_by":1,"name":"Mustafa Kokce","email":"","orcid":"","institution":"","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Mustafa","middleName":"","lastName":"Kokce","suffix":""},{"id":288414017,"identity":"a1e3fd06-ca53-495e-b693-b371828c8007","order_by":2,"name":"Mert Çetin","email":"","orcid":"","institution":"","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Mert","middleName":"","lastName":"Çetin","suffix":""},{"id":288414018,"identity":"456bd2fc-e6ba-4e29-9075-95c182ce4d0f","order_by":3,"name":"Kemal Türker","email":"","orcid":"","institution":"","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Kemal","middleName":"","lastName":"Türker","suffix":""},{"id":288414019,"identity":"3f13bd34-1209-4c5d-8371-2c13b207861b","order_by":4,"name":"Ilhan Karacan","email":"","orcid":"","institution":"Istanbul Physical Therapy Rehabilitation Training and Research Hospital","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Ilhan","middleName":"","lastName":"Karacan","suffix":""}],"badges":[],"createdAt":"2024-03-27 23:00:58","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4178539/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4178539/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":54450312,"identity":"bbe17ce0-7c86-4c07-8392-12e33823dfdb","added_by":"auto","created_at":"2024-04-10 17:43:55","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":3211599,"visible":true,"origin":"","legend":"\u003cp\u003eBoth M waves and H-reflexes are observed in the TA muscle sEMG and MMU EMG recordings during tibial nerve stimulation in a control. Arrows indicate the moment of electrical stimulation. Gray bands indicate the time period of the M-response or H-reflex.\u003c/p\u003e","description":"","filename":"Fig1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4178539/v1/ff7bcf8be290c16de4fe2387.jpg"},{"id":54450313,"identity":"f7ac0577-ecdd-45a0-9b52-27c4742c4a92","added_by":"auto","created_at":"2024-04-10 17:43:55","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":5525357,"visible":true,"origin":"","legend":"\u003cp\u003eBoth M waves and H-reflexes are observed in the TA muscle sEMG and MMU EMG recordings during tibial nerve stimulation in an individual with SCL. Arrows indicate the moment of electrical stimulation. Gray bands indicate the time period of the M-response or H-reflex. \u003cstrong\u003e(a)\u003c/strong\u003e The records were taken with 18mA electric current stimulation. H-reflex responses are observed in all recordings. \u003cstrong\u003e(b)\u003c/strong\u003e The recordings were taken with 40mA electric current stimulation. In all recordings, M responses are still present but the H-reflex has disappeared.\u003c/p\u003e","description":"","filename":"Fig2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4178539/v1/ee9139dfcbd8bb911af9c8c0.jpg"},{"id":54450314,"identity":"06828e5c-3d52-4be4-aced-a7b72dfcb3bc","added_by":"auto","created_at":"2024-04-10 17:43:55","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":3851667,"visible":true,"origin":"","legend":"\u003cp\u003eT-reflex and mechanical artifact after striking the Achilles tendon. (a) Reflex latencies were recorded with MMU and sEMG electrodes. The solid vertical line represents the moment of impact on the Achilles tendon. Arrows indicate the starting point of the T-reflex response. (b) By optimizing the y-axis of the MMU EMG channels, mechanical artifacts in the tibialis anterior and soleus muscles were made visible. The solid thick vertical line denotes the moment of impact on the Achilles tendon, the dashed line indicates the moment of appearance of the artifact recorded in the soleus MMU, and the thin solid line indicates the moment of appearance of the artifact recorded in the tibialis anterior MMU. Acc: Accelerometer TA: Tibialis anterior, au: arbitrary unit\u003c/p\u003e","description":"","filename":"Fig3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4178539/v1/3a229e4b842ef57326a26d17.jpg"},{"id":61572616,"identity":"5db15cdc-9bfa-4959-a200-6d162a79e2da","added_by":"auto","created_at":"2024-08-01 11:19:49","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":13160348,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4178539/v1/224a9e52-b9f9-49bc-b0a5-979f7fa1290d.pdf"}],"financialInterests":"There is no duality of interest","formattedTitle":"Is Reciprocal Facilitation a Myth in Upper Motor Neuron Lesions?","fulltext":[{"header":"1. Introduction","content":"\u003cp\u003eSherrington described reciprocal innervation as the spinal mechanism regulating the movements of agonist and antagonist muscle groups. It involves the activation of an agonist motor neuron pool, which leads to the inhibition of the corresponding antagonist motor neuron pool. This process ensures that while agonists contract, antagonists relax, allowing coordinated movement [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eReciprocal (antagonist) inhibition involves a disynaptic circuit in the spinal cord, influenced by various supraspinal and segmental modulatory mechanisms [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e]. Additionally, presynaptic inhibition and other neural mechanisms have been proposed to contribute to antagonist inhibition [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e, \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. Disruptions in antagonist inhibition are a notable characteristic of human spasticity, wherein involuntary co-contractions of antagonist muscles frequently occur instead of selective activation of agonists [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e]. The occurrence of co-contraction in the spastic limb is attributed to the disappearance of antagonist inhibition and the emergence of reciprocal facilitation in its place [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. However, convincing evidence supporting this hypothesis is currently lacking. Reciprocal Ia inhibition can either increase, decrease, or disappear entirely, depending on various factors such as the underlying cause of the disease, the location of the lesion, the severity of spasticity, and the extent of functional recovery [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eWhile antagonist inhibition/facilitation is straightforward, identifying reciprocal inhibition/facilitation poses more challenges. There are some electrophysiological studies, however, that support reciprocal facilitation where reflex responses were captured using surface EMG (sEMG) [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. Nonetheless, a notable limitation of sEMG is the potential for crosstalk In sEMG, signals from agonist reflex muscles may inadvertently be recorded by antagonist muscle electrodes, giving a false impression that the reflex responses are coming from the antagonist muscle. Multi-motor unit (MMU) EMG is widely recognized as reliable for identifying crosstalk as it records action potentials of active motor units from a small portion of the muscle of interest [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. Using the MMU EMG technique, this study tests whether reciprocal facilitation is an erroneous interpretation resulting from crosstalk. Establishing the validity of electrophysiological evidence indicating the emergence of the reciprocal facilitation phenomenon in upper motor neuron lesions is crucial. Specific anti-spastic treatment methods, like cold therapy and proprioceptive neuromuscular stimulation, use the concept of antagonist inhibition [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. However, suppose reciprocal facilitation proves to be a valid phenomenon. In that case, it will significantly impact the development of new treatment methods for patients suffering from upper motor neuron lesions.\u003c/p\u003e"},{"header":"2. Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003e2.1. Participants\u003c/h2\u003e \u003cp\u003eIn this quasi-experimental study, five individuals with chronic incomplete spinal cord lesions (SCL) participated, with an average age of 46.8 years (\u0026plusmn;\u0026thinsp;16.5), comprising 4 females and 1 male. Additionally, five able-bodied volunteers took part, with an average age of 28.6 years (\u0026plusmn;\u0026thinsp;3.3), including 3 females and 2 males. Patients with premorbid neuromuscular disease or a history of autonomic dysreflexia were not included in the study. All participants provided informed consent prior to participation. All experimental procedures were designed with the Helsinki Declaration in mind and were approved by the local ethics committee (Approval Number: 2022-17-19). The study protocol was registered with ClinicalTrials.gov (NCT05985031).\u003c/p\u003e \u003cp\u003eThe average duration of spinal cord injury was 9.4 years, ranging from 5 to 15 years. All individuals with SCL were classified as paraplegic. Among them, four had traumatic SCL and one had a non-traumatic SCL. Two were classified as AIS (ASIA (American Spinal Injury Association) Impairment Scale) C class, and three were classified as AIS D class. Using the modified Ashworth scale, soleus spasticity was rated as score 1 in one case, 1\u0026thinsp;+\u0026thinsp;in three cases, and score 2 in one case.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003e2.2. Procedures\u003c/h2\u003e \u003cp\u003eIn the present study, to evoke the tibialis anterior muscle reciprocal facilitation response, the Soleus T-reflex was elicited by tapping the Achilles tendon, while the Soleus H-reflex was elicited by stimulating the tibialis nerve. Participants were positioned safely and comfortably in a prone position on the examination table. Reflex responses were recorded simultaneously from the right soleus and right tibialis anterior muscles using both sEMG and MMU EMG.\u003c/p\u003e \u003cdiv id=\"Sec5\" class=\"Section3\"\u003e \u003ch2\u003e2.2.1. \u003cem\u003eEliciting the soleus reflex response\u003c/em\u003e\u003c/h2\u003e \u003cp\u003eTo elicit the soleus T-reflex, fifteen consecutive strokes of constant intensity were applied to the right Achilles tendon with the ankle in a neutral position. To prevent the development of depression after homosynaptic activation in patients with upper motor neuron lesions, it is recommended to maintain a minimum interval of 10 seconds between successive stimulations [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e]. In this study, the time between tendon strokes was kept longer than 10 seconds.\u003c/p\u003e \u003cp\u003eTo elicit the soleus H-reflex, the right tibial nerve was stimulated using a monopolar technique with a square-shaped monophasic electric current featuring a pulse duration of 1 ms. The anode, sized 10x10 cm, was positioned on the suprapatellar region, while the cathode electrode, with a diameter of 1 cm and hemispherical in shape, was placed on the tibial nerve at the midpoint of the fold line in the popliteal fossa. Electrocardiography (ECG) gel was applied beneath the electrodes to enhance conductivity, and the electrodes were securely affixed to the skin. The rest period between successive electrical stimulations was at least 10 seconds. Electrical stimulations were administered using a constant current generator (model DS7A, Digitimer Ltd, Hertfordshire, UK).\u003c/p\u003e \u003cp\u003eA recruitment curve was generated for each participant by gradually increasing the stimulus intensity. This process identified the current intensities corresponding to the onset of the H-reflex (Hmin), the minimum M-response (Mmin), and the disappearance of the H-reflex alongside the attainment of the maximum M-response (Mmax). The range of current intensity that elicited the Hmin and Mmax responses from the right tibial nerve was divided into ten equal increments. At each intensity level, the right tibial nerve underwent stimulation via the popliteal fossa five times. Simultaneously, monitoring was conducted to identify any instances of reciprocal facilitation in the Tibialis anterior muscle sEMG and MMU EMG recordings.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section3\"\u003e \u003ch2\u003e2.2.2. \u003cem\u003eData recording\u003c/em\u003e\u003c/h2\u003e \u003cp\u003eA pair of self-adhesive Ag/AgCl (Redline\u0026reg;) electrodes were applied to the skin following the SENIAM protocol to obtain superficial EMG recordings from the right soleus and tibialis anterior muscles using the bipolar technique [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. The ground electrode was affixed to the right lateral malleolus. Before applying the electrodes, any hair on the skin was shaved, the skin was lightly abraded to remove dead skin using sandpaper, and the skin surface was cleaned with alcohol wipes to remove any oil residue. ECG gel was then applied to the skin area beneath the electrodes to increase skin moisture, ensuring skin resistance between the electrodes remained below 10 kOhm.\u003c/p\u003e \u003cp\u003eTo record soleus and tibialis anterior EMG signals using MMU EMG, a pair of silver wire electrodes (75 \u0026micro;m core diameter) insulated with Teflon, except for the cut ends, was utilized. These wires were threaded through the channel of a 25 G needle, and their ends were shaped like fishhooks, with a distance of approximately 3 mm between them. The pair of wires was inserted between two surface EMG electrodes into the muscle to a depth of about 3 cm, using the needle. The needle was then removed, leaving the fishhooked wires inside the muscle. A lip-clip electrode served as the ground electrode [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eAn accelerometer (LIS344ALH, \u0026plusmn;\u0026thinsp;6 g full-scale range, linear accelerometer, ECOPACK\u0026reg;, Mansfield, TX, USA) was employed to measure the latency of the Achilles tendon reflex.\u003c/p\u003e \u003cp\u003eAll EMG and accelerometer recordings were obtained using a data recorder (CED 1902 Quad System MKIII amplifier and CED 3601 Power 1401 MKII digital-to-analog converter, Cambridge Electronic Design Limited, Cambridge, England) and analyzed using software (Cambridge Electronic Designs Spike2\u0026reg;). The sampling rate for recordings was set at 2 kHz for sEMG and accelerometer data, and 10 kHz for MMU EMG recordings.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section3\"\u003e \u003ch2\u003e2.2.3.Data Analysis\u003c/h2\u003e \u003cp\u003e \u003cb\u003eDetection of reciprocal facilitation\u003c/b\u003e \u003c/p\u003e \u003cp\u003eAll EMG and accelerometer recordings underwent processing with infinite impulse response filters (Butterworth, 2nd order). The sEMG recordings were filtered using a 20\u0026ndash;500 Hz band-pass filter, while the intramuscular recordings were filtered using a 100\u0026ndash;5000 Hz band-pass filter. Spike-triggered averaging was conducted using the onset point as the trigger and the electrical signals recorded by EMG electrodes as the source to assess reciprocal facilitation. This procedure entailed averaging 5 ms of filtered EMG data before the trigger and 50 ms after it.\u003c/p\u003e \u003cp\u003e \u003cb\u003eExtraction of motion artifact signals\u003c/b\u003e \u003c/p\u003e \u003cp\u003eThe onset point of the tap-induced mechanical stimulus was visually marked on the accelerometer recording. This onset point served as the trigger for spike-triggered averaging, using the electrical signals recorded by MMU electrodes as the source. Spike-triggered averaging aimed to extract motion artifact signals from the total background tension generated by the asynchronous firing of active synergist motor units. The exact onset of the mechanical artifact in the averaged EMG recordings was determined using the CUSUM method [\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e].\u003c/p\u003e \u003cp\u003e \u003cb\u003eMeasurement of T- reflex latency\u003c/b\u003e \u003c/p\u003e \u003cp\u003eAn accelerometer was affixed to the Achilles tendon to assess the timing and intensity of tendon tapping with the reflex hammer. The raw reflex latency was determined as the period between the onset of impact on the tendon, detected by the accelerometer, and the onset of the T-reflex in the sEMG recordings. These measurements were adjusted for the delay of the mechanical artifact, identified using MMU electrodes. The duration for mechanical stimulation to reach the soleus and tibialis anterior muscle belly was determined, subtracted from the raw T-reflex latencies, and reported as T-reflex latency in the \u003cspan refid=\"Sec10\" class=\"InternalRef\"\u003eResults\u003c/span\u003e section.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section3\"\u003e \u003ch2\u003e2.2.4.Outcome measures\u003c/h2\u003e \u003cp\u003eThe primary outcome measures of this study include the H-reflex, M-wave, and T-reflex. The secondary outcome measure was the mechanical artifact induced by the reflex hammer during the tap on the Achilles tendon.\u003c/p\u003e \u003cp\u003eThe interpretations of the H-reflex and M-response findings in both muscle sEMG and MMU-EMG recordings are as follows: reciprocal facilitation, cross-talk, or direct stimulation of the peroneal nerve (Cross-electrical stimulation) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eThe interpretations of the findings of H-reflex studies\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"5\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eScenarios\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eSoleus sEMG /\u003c/p\u003e \u003cp\u003eMMU EMG\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c4\" namest=\"c3\"\u003e \u003cp\u003eTibialis anterior\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eInterpretation\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003esEMG\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMMU EMG\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eScenario \u0026minus;\u0026thinsp;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eReciprocal facilitation\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eM-wave (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eM-wave (-)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eM-wave (-)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eScenario \u0026minus;\u0026thinsp;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eH-reflex (-)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eCross-talk\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eM-wave (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eM-wave (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eM-wave (-)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eScenario \u0026minus;\u0026thinsp;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eH-reflex (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eCross-stimulation\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eM-wave (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eM-wave (+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eM-wave (+)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"5\"\u003esEMG: Surface EMG, MMU: multi-motor unit\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eThe interpretations of the T-reflex in both muscle sEMG and MMU-EMG recordings are as follows: reciprocal facilitation, cross-talk, or tibialis anterior muscle spindle stimulation (cross-mechanical stimulation)(Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eThe interpretations of the findings of Achilles tendon T-reflex studies\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eScenarios\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eTA T-reflex\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eMechanical artifact\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTiming the TA T-reflex\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eInterpretation\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003esEMG\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMMU\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eScenario \u0026minus;\u0026thinsp;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e(+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e(+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eAfter soleus T-reflex\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eReciprocal facilitation\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eScenario \u0026minus;\u0026thinsp;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e(+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e(-)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eAfter soleus T-reflex\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eCross-talk\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eScenario \u0026minus;\u0026thinsp;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e(+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e(+)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eAfter/before soleus T-reflex\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003ecross-stimulation\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"6\"\u003esEMG: Surface EMG, MMU: multi-motor unit\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003e2.3.Statistical Analysis\u003c/h2\u003e \u003cp\u003eThe normality of the data was assessed using the Shapiro-Wilk test. Continuous variables were presented as mean and standard deviation, while categorical variables were expressed as frequencies. Group means were compared using the Mann-Whitney U test. The Fisher exact probability test was employed to analyze the distribution of categorical variables among groups. The statistical significance was set at p\u0026thinsp;\u0026lt;\u0026thinsp;0.05. The software package used for data management was PASW Statistics for Windows, Version 18.0 [SPSS Inc, Armonk, NY].\u003c/p\u003e \u003c/div\u003e"},{"header":"2. Results","content":"\u003cp\u003eIn all individuals with SCL and all healthy controls, stimulation of the tibial nerve elicited an M wave with an H reflex in the tibialis anterior muscle; this suggests simultaneous direct stimulation of the peroneal nerve as well as the tibial nerve (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, \u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e indicates that in individuals with SCL, the tibialis anterior H-reflex appeared on average 0.5 ms before the Soleus H-reflex, while in the Control group, the tibialis anterior H-reflex appeared on average 1.5 ms before the Soleus H-reflex.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eH-reflex studies findings in sEMG and MMU EMG\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"9\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eGroup\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eSubject\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c4\" namest=\"c3\"\u003e \u003cp\u003eTA H-reflex\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c6\" namest=\"c5\"\u003e \u003cp\u003eTA M-wave\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"3\" nameend=\"c9\" namest=\"c7\"\u003e \u003cp\u003eH-reflex latency (ms)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003esEMG\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMMU\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003esEMG\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eMMU\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eTibialis anterior\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003eSoleus\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003eDifference\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"4\" rowspan=\"5\"\u003e \u003cp\u003eSCL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e30.75\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e31.64\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-0.89\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e24.55\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e24.98\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-0.43\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e29.71\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e30.84\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-1.13\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e30.11\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e30.25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-0.14\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e31.80\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e31.69\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e0.11\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"4\" rowspan=\"5\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e31.17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e31.84\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-0.67\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e28.05\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e29.53\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-1.48\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e27.62\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e28.68\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-1.06\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e28.40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e30.66\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-2.26\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e27.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e29.16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-2.12\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"9\"\u003eTA: Tibialis anterior, sEMG: surface EMG, MMU: multi-motor unit\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eWhen the Achilles tendon was struck with a reflex hammer, T-reflex responses occurred along with mechanical stimulation artifacts in both the soleus and tibialis anterior muscles in all cases (Table\u0026nbsp;\u003cspan refid=\"Tab4\" class=\"InternalRef\"\u003e4\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The mechanical artifact reached the tibialis anterior MMU electrodes approximately 0.6 ms later in the SCL group and 0.9 ms later in the Control group compared to the soleus MMU electrodes. The T-reflex latency calculated based on the artifact was found to be 1.2 ms shorter in the SCL group and 2.2 ms shorter in the Control group compared to the soleus muscle in the tibialis anterior muscle (Table\u0026nbsp;\u003cspan refid=\"Tab4\" class=\"InternalRef\"\u003e4\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab4\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 4\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eFindings of T-reflex studies in sEMG and MMU EMG and artifact in MMU EMG\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"10\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eGroup\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eSubject\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c4\" namest=\"c3\"\u003e \u003cp\u003eTA T-reflex\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\" morerows=\"1\" rowspan=\"2\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c7\" namest=\"c6\"\u003e \u003cp\u003eArtifact latency (ms)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c10\" namest=\"c8\"\u003e \u003cp\u003eReflex latency (ms)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003esEMG\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMMU\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eTA artifact\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003eSoleus artifact\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c8\"\u003e \u003cp\u003eTA\u003c/p\u003e \u003cp\u003eT-reflex\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c9\"\u003e \u003cp\u003eSoleus\u003c/p\u003e \u003cp\u003eT- reflex\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c10\"\u003e \u003cp\u003eDifference\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSCL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNA\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e1.83\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e1.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e35.23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e37.49\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-2.26\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.21\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e2.63\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e25.08\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e26.34\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-1.26\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.46\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e1.70\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e32.69\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e34.33\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-1.65\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e3.23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e1.96\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e34.67\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e35.26\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-0.59\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e2.15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e32.71\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e32.99\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-0.27\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e3.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e2.29\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e34.16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e35.00\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-0.83\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e1.88\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e 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\u003cp\u003e3.27\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e28.39\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e32.34\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-3.95\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e2.84\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e1.57\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e31.54\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e35.54\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-4.01\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e+\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e1.92\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c7\"\u003e \u003cp\u003e1.51\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e31.08\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e31.89\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c10\"\u003e \u003cp\u003e-0.81\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"10\"\u003eTA: Tibialis anterior\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"3. Discussion","content":"\u003cp\u003eUnlike previous studies that examined the presence of reciprocal facilitation, this study, which included MMU EMG recordings in addition to sEMG, revealed two original findings: First, during the H-reflex study, the electrical current applied to stimulate the tibial nerve in the popliteal fossa also inadvertently stimulates the peroneal nerve nearby, a phenomenon termed cross-stimulation. Second, in the T-reflex study, when the Achilles tendon is tapped with a reflex hammer to elicit the soleus T-reflex, the resulting mechanical stimulation spreads to the belly of the tibialis anterior muscle, activating the muscle spindles and eliciting the tibialis anterior T-reflex response. Ultimately, no evidence supporting reciprocal facilitation was found.\u003c/p\u003e \u003cp\u003e \u003cb\u003eMethodological Considerations\u003c/b\u003e \u003c/p\u003e \u003cp\u003eXia and Rymer examined changes in the antagonist inhibition patterns between agonist and antagonist muscles of the ankle in individuals with complete SCL and incomplete SCL [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. Their study, which included eight participants in each group, investigated these pattern changes under four specific conditions. These conditions involved applying a reflex hammer to either the tibialis anterior tendon or the Achilles tendon while the ankle was in full dorsiflexion or full plantar flexion. As a result, it has been reported that the reciprocal facilitation pattern is most frequently observed in cases with incomplete SCL by tapping the Achilles tendon during foot dorsiflexion (reciprocal facilitation in six out of eight cases in their study). Therefore, in this study, reciprocal facilitation was tested by performing an Achilles tendon hit in individuals with incomplete SCL.\u003c/p\u003e \u003cp\u003eUnlike previous electrophysiological studies [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e, \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e], this study involved both T-reflex and H-reflex tests, rather than focusing solely on the T-reflex or H-reflex alone.\u003c/p\u003e \u003cp\u003eGiven that the primary objective of this study was to discern whether reciprocal facilitation stemmed from cross-talk, a departure from prior research was made by incorporating MMU EMG electrode recordings alongside sEMG recordings. Cross-talk, a significant source of error, arises from electrical signals originating from adjacent muscles. Compared to sEMG, the MMU EMG technique boasts a superior signal-to-noise ratio, capturing signals from highly localized muscle areas. Consequently, MMU EMG serves as an effective safeguard against electrical signals (cross-talk) emanating from neighboring muscles [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. Tests were also conducted on able-bodied volunteers to make comparisons in terms of cross-talk.\u003c/p\u003e \u003cp\u003e \u003cb\u003eReciprocal facilitation vs Cross-talk or Cross-stimulation\u003c/b\u003e \u003c/p\u003e \u003cp\u003eThe inspiration for this research stemmed from Xia and Rymer's article [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e], where they discussed the potential for cross-talk issues. However, it appears that no specific precautions were implemented in their research methodology to address this concern. In contrast, the present study utilized the MMU-EMG recording technique, which effectively discerns whether cross-talk is occurring [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. Indeed, this study revealed that the primary concern is not cross-talk but rather cross-mechanical stimulation.\u003c/p\u003e \u003cp\u003eIn their study, Topkara et al. demonstrated that mechanical stimulation applied to the calcaneus extended not only to the soleus muscle but also to the quadriceps muscle, and this mechanical artifact was detectable using MMU electrodes [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]. When the Achilles tendon is struck with a reflex hammer, the resulting mechanical vibrations propagate through the soleus muscle, stimulating the muscle spindles and triggering the soleus T-reflex response. Moreover, in the present study, MMU EMG recordings revealed that mechanical stimuli also spread to the tibialis anterior muscle belly upon striking the Achilles tendon with a reflex hammer. It was determined that mechanical stimuli reached the tibialis anterior MMU electrodes within a time frame varying between 1.88–4.91 ms, and the soleus MMU electrodes within a time frame varying between 1.07–3.27 ms. If it had been observed that the TA T-reflex response occurred before the soleus T-reflex response when the Achilles tendon was struck, it would have been strong evidence for the view that the mechanical artifact stimulated the TA muscle spindles and triggered the T-reflex. However, the fact that the mechanical stimulus reaches the tibialis anterior muscle later than the soleus muscle and that the tibialis anterior T-reflex latency is shorter than the soleus T-reflex latency creates a complex picture that makes interpretation difficult.\u003c/p\u003e \u003cp\u003eIn controlled studies by Okuma et al. on five incomplete SCL patients and by Crone et al. on 11 SCL patients and six hemiplegic patients, it was reported that a reciprocal facilitation response occurred in the tibialis anterior muscle with tibial nerve stimulation [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e, \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]. In both studies, the tibial nerve was stimulated using the monopolar technique, similar to the method employed in the current study. Here, recordings were conducted using MMU electrodes, revealing that when the tibial nerve was stimulated with the monopolar technique, the peroneal nerve was simultaneously and directly stimulated (cross-stimulation phenomenon). The presence of an M response in MMU-EMG recordings, in addition to sEMG recordings, during tibial nerve stimulation serves as definitive evidence against the occurrence of cross-talk or reciprocal facilitation. If a reciprocal stimulation response had indeed occurred, only an H-reflex-like EMG response would have been observed without an M response. Conversely, in the case of cross-talk, M-wave and H-reflex responses would be observed in sEMG recordings, but not in MMU-EMG recordings.\u003c/p\u003e \u003cp\u003e \u003cb\u003eLimitation\u003c/b\u003e \u003c/p\u003e \u003cp\u003eThe number of individuals with incomplete SCL in this study may be considered small. As mentioned above, the frequency of antagonist inhibition among individuals with incomplete SCL was reported as 6/8 in the study by Xia and Rymer [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. However, it's important to note that our study is not focused on the prevalence and clinical features of reciprocal facilitation; rather, it aims to assess the reliability of neurophysiological methods used to demonstrate its presence.\u003c/p\u003e "},{"header":"Conclusion","content":"\u003cp\u003eThis study concluded that there were no findings supporting reciprocal facilitation. In H-reflex studies, it was shown for the first time that during stimulation of the tibial nerve with electrical current, the peroneal nerve was also stimulated (cross-electrical stimulation). In T-reflex studies, it has been demonstrated that when the tendon of the agonist muscle is struck, the antagonist muscle, as well as the agonist muscle, can be stimulated (cross-mechanical stimulation). However, due to the significant limitations (i.e., cross-stimulation) observed in H-reflex and T-reflex-based reciprocal facilitation tests, this study did not provide evidence supporting the existence of reciprocal facilitation in patients with SCL. Nevertheless, the findings of this study do not completely rule out the phenomenon of reciprocal facilitation in patients with upper motor neuron disease. Electrophysiological studies that provide solutions to the cross-stimulation problem are needed to definitively reveal the development of the reciprocal facilitation phenomenon in patients with upper motor lesions. Antagonist inhibition is the mainstay of approaches such as anti-spastic treatment with proprioceptive neuromuscular stimulation, ice applied to the antagonist muscle, and neuromuscular electrical stimulation in patients with upper motor neuron lesions [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. Hence, it is crucial to elucidate the transition from antagonist inhibition to reciprocal facilitation in this context.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e \u003ch2\u003eCOMPETING INTERESTS\u003c/h2\u003e \u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e \u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eSherrington CS. The Integrative Action of the Nervous System. Yale University Press, New Haven. 1906.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol. 1992; 38:335\u0026ndash;378.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eEl-Tohamy A, Sedgwick EM. Spinal inhibition in man: depression of the soleus H reflex by stimulation of the nerve to the antagonist muscle. J Physiol. 1983; 337:497\u0026ndash;508.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFu TC, Hultborn H, Larsson R, Lundberg A. Reciprocal inhibition during the tonic stretch reflex in the decerebrate cat. J Physiol. 1978; 284:345\u0026ndash;369\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAshby P, Wiens M. Reciprocal inhibition following lesions of the spinal cord in man. J Physiol. 1989; 414:145\u0026ndash;157.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBoorman G, Hulliger M, Lee RG, Tako K, Tanaka R. Reciprocal Ia inhibition in patients with spinal spasticity. Neurosci Lett. 1991; 127:57\u0026ndash;60.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCrone C, Johnsen LL, Biering-S\u0026oslash;rensen F, Nielsen JB. Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain. 2003; 126:495\u0026ndash;507.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eXia R, Rymer WZ. Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord. 2005; 43:14\u0026ndash;21.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCremoux S, Amarantini D, Tallet J, Dal Maso F, Berton E. Increased antagonist muscle activity in cervical SCI patients suggests altered reciprocal inhibition during elbow contractions. Clin Neurophysiol. 2016; 127:629\u0026ndash;634.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOkuma Y, Mizuno Y, Lee RG. Reciprocal Ia inhibition in patients with asymmetric spinal spasticity. Clin Neurophysiol. 2002; 113:292\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eT\u0026uuml;rker KS, Miles TS. Cross-talk from other muscles can contaminate EMG signals in reflex studies of the human leg. Neurosci Lett. 1990; 111:164\u0026ndash;169.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWhitney SL. Physical Agents: Heat and Cold Modalities. In: Scully RM, Barnes MR (Eds), Physical Therapy. JB Lippincott Co Philadelphia 1989: 849\u0026ndash;852\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSahin N, Ugurlu H, Albayrak I. The efficacy of electrical stimulation in reducing the post-stroke spasticity: a randomized controlled study. Disabil Rehabil. 2012; 34:151\u0026ndash;156.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRing H, Weingarden H. Neuromodulation by functional electrical stimulation (FES) of limb paralysis after stroke. Acta Neurochir Suppl. 2007; 97:375\u0026ndash;380.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eYurttutmuş Z, Ekici Zincirci D, Bardak AN, Topkara B, Aydın T, Karacan I, et al. A stimulus rate that is not influenced by homosynaptic post-activation depression in chronic stroke. Somatosens Mot Res. 2020; 37:271\u0026ndash;276.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000; 10:361\u0026ndash;374.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBrinkworth RS, T\u0026uuml;rker KS. A method for quantifying reflex responses from intra-muscular and surface electromyogram. J Neurosci Methods. 2003;122:179\u0026ndash;93. doi: \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003e10.1016/s0165-0270(02)00321-7\u003c/span\u003e\u003cspan address=\"10.1016/s0165-0270(02)00321-7\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eT\u0026uuml;rker KS. Electromyography: some methodological problems and issues. Phys Ther. 1993; 73:698\u0026ndash;710.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eEllaway PH. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol. 1978; 45:302\u0026ndash;304.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOkuma Y, Lee RG. Reciprocal inhibition in hemiplegia: correlation with clinical features and recovery. Can J Neurol Sci. 1996; 23:15\u0026ndash;23.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCrone C, Johnsen LL, Nielsen J. Reciprocal inhibition in hemiplegic patients\u0026ndash;a longitudinal study. Suppl Clin Neurophysiol. 2000; 53:187\u0026ndash;191.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTopkara B, Aydin T, Corum M, Karaoglu A, Ekici Zincirci D, S Bugdayci D, et al. A new method to determine stretch reflex latency. Muscle Nerve. 2021;64:726\u0026ndash;733.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"spinal cord injury, paraplegia, tetraplegia, reciprocal inhibition","lastPublishedDoi":"10.21203/rs.3.rs-4178539/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4178539/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eStudy Design:\u003c/strong\u003e Clinical trial\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eObjective: \u003c/strong\u003eTo investigate whether reciprocal facilitation is a pseudo-reflex response resulting from crosstalk or cross-stimulation using the MMU EMG technique.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eSetting: \u003c/strong\u003eIstanbul Physical Therapy Rehabilitation Training and Research Hospital, Istanbul, Turkiye\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMethods: \u003c/strong\u003eFive individuals with chronic incomplete spinal cord lesions (SCL) and five able-bodied volunteers participated in the study. To trigger the reciprocal facilitation response in the tibialis anterior muscle, the Soleus T-reflex was induced by tapping the Achilles tendon, while the Soleus H-reflex was elicited by stimulating the tibialis nerve. Reflex responses were simultaneously recorded from the right soleus and right tibialis anterior muscles using both surface electromyography (sEMG) and multi-motor unit (MMU) EMG.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults: \u003c/strong\u003eIt was noted that the EMG responses initially interpreted as reciprocal facilitation in both able-bodied individuals and those with SCL were actually due to cross-stimulation. Specifically, it was found that when the tibial nerve was stimulated with an electrical current to evoke the soleus H-reflex, simultaneous stimulation of the peroneal nerve occurred, resulting in the occurrence of both tibialis anterior H-reflex and M wave (cross-electrical stimulation). Additionally, striking the Achilles tendon with a reflex hammer to elicit the soleus T-reflex resulted in mechanical stimulation spreading to both the soleus and tibialis anterior muscle bellies, activating the muscle spindles and eliciting both soleus and tibialis anterior T-reflex responses (cross-mechanical stimulation).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusions: \u003c/strong\u003eNo evidence supporting reciprocal facilitation was found. Further research utilizing H-reflex and T-reflex tests, resolving the cross-stimulation issue, is needed to establish its existence conclusively.\u003c/p\u003e","manuscriptTitle":"Is Reciprocal Facilitation a Myth in Upper Motor Neuron Lesions?","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-04-10 17:43:50","doi":"10.21203/rs.3.rs-4178539/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"12add949-1236-4d6b-907c-dc49724c468e","owner":[],"postedDate":"April 10th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":30364369,"name":"Health sciences/Neurology/Neurological disorders/Movement disorders"},{"id":30364370,"name":"Biological sciences/Neuroscience/Motor control"}],"tags":[],"updatedAt":"2024-08-01T11:11:37+00:00","versionOfRecord":[],"versionCreatedAt":"2024-04-10 17:43:50","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4178539","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4178539","identity":"rs-4178539","version":["v1"]},"buildId":"cBFmMYwuxLRRLfASyISRj","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}