ROSPECTS FOR THE USE OF H-REFLEXOMETRY IN THE STUDY OF HUMAN MOTOR FUNCTION
DOI:
https://doi.org/10.11603/1811-2471.2024.v.i1.14522Keywords:
H-reflex, H-reflexometry, muscleAbstract
SUMMARY. The article application of H-reflexometry in the study of the central mechanisms of random human movements, which is mainly carried out on healthy subjects, is demonstrated. It has been shown that the results of clinical trials performed by H-reflexometry with the participation of injured people or people with neurological disorders provide additional information about these mechanisms, reveal the causes of human motor function disorders, contribute to the improvement of methods of their study and provide opportunities for the implementation of rehabilitation measures.
The aim – to evaluate the prospects of using H-reflexometry in the study of central mechanisms of movements and means of restoring and maximizing the motor capabilities of people.
Material and Methods. The analysis was carried out using the scientific biological and medical information search system PubMed.
Results. H-reflexometry was used both for the study of motor functions of healthy people and patients with injuries and neurological disorders. The authors studied mainly H-reflexes m.soleus, m. flexor carpi radialis, m. quadriceps. The total number of publications with the results of studies performed on other muscles indicates the possibility of a wider use of H-reflexometry in the study of motor functions in humans than is generally accepted and currently implemented. It was found that H-reflexometry was used to the greatest extent in the researches of the mechanisms of motor disorders arising as a result of stroke and spinal cord injuries.
Conclusions. The results of the review indicate that H-reflexometry provides ample opportunities to study human motor function in normal and pathological conditions, and it may be especially promising at present to examine injured people using this method, to implement and monitor their rehabilitation measures.
References
Burke, D. (2016). Clinical uses of H reflexes of upper and lower limb muscles. Clinical neurophysiology practice, 1, 9-17. DOI: 10.1016/j.cnp.2016.02.003.
Theodosiadou, A., Henry, M., Duchateau, J., & Baudry, S. (2023). Revisiting the use of Hoffmann reflex in motor control research on humans. European journal of applied physiology, 123(4), 695-710. DOI: 10.1007/s00421-022-05119-7.
Stålberg, E., van Dijk, H., Falck, B., Kimura, J., Neuwirth, C., Pitt, M., Podnar, S., Rubin, D. I., Rutkove, S., Sanders, D. B., Sonoo, M., Tankisi, H., & Zwarts, M. (2019). Standards for quantification of EMG and neurography. Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology, 130(9), 1688-1729. DOI: 10.1016/j.clinph.2019.05.008.
Norton, J.J.S., & Wolpaw, J.R. (2018). Acquisition, Maintenance, and Therapeutic Use of a Simple Motor Skill. Current opinion in behavioral sciences, 20, 138-144. DOI: 10.1016/j.cobeha.2017.12.021.
Pearcey, G.E.P., & Zehr, E.P. (2019). Exploiting cervicolumbar connections enhances short-term spinal cord plasticity induced by rhythmic movement. Experimental brain research, 237(9), 2319-2329. DOI: 10.1007/ s00221-019-05598-9.
Wecht, J.R., Savage, W.M., Famodimu, G.O., Mendez, G., Levine, J.M., Maher, M.T., Weir, J.P., Wecht, J.M., Carmel, J.B., Wu, Y.K., & Harel, N.Y. (2021). Posteroanterior Cervical Transcutaneous Spinal Cord Stimulation: Interactions with Cortical and Peripheral Nerve Stimulation. Journal of clinical medicine, 10(22), 5304. DOI: 10.3390/jcm10225304.
Khosrawi, S., Vahdatpour, B., & Ahmadi, M. (2018). Evaluation of Relationship between Extensor Digitorum Communis Hoffmann-reflex Latency and Upper Limb Length and Age. Advanced biomedical research, 7, 65. DOI: 10.4103/abr.abr_106_17.
Krüger, M., & Lux, V. (2023). Failure of motor function-A Developmental Embodiment Research perspective on the systemic effects of stress. Frontiers in human neuroscience, 17, 1083200. DOI: 10.3389/fnhum.2023.1083200.
Aagaard, P. (2018). Spinal and supraspinal control of motor function during maximal eccentric muscle contraction: Effects of resistance training. Journal of sport and health science, 7(3), 282-293. DOI: 10.1016/j.jshs.2018. 06.003.
Song, Q., Sun, M., Lewis, K., Choi, J. H., Manor, B., & Li, L. (2022). Hoffmann Reflex Measured From Lateral Gastrocnemius Is More Reliable Than From Soleus Among Elderly With Peripheral Neuropathy. Frontiers in aging neuroscience, 14, 800698. DOI: 10.3389/fnagi.2022. 800698.
Sun, M., Lewis, K., Choi, J.H., Zhang, F., Qu, F., & Li, L. (2022). The Reduced Adaptability of H-Reflex Parameters to Postural Change With Deficiency of Foot Plantar Sensitivity. Frontiers in physiology, 13, 890414. DOI: 10.3389/ fphys.2022.890414.
Sun, M., Zhang, F., Lewis, K., Song, Q., & Li, L. (2022). The Impact of Hoffmann Reflex on Standing Postural Control Complexity in the Elderly with Impaired Plantar Sensation. Entropy (Basel, Switzerland), 25(1), 64. DOI: 10.3390/e25010064.
Ghasemi, E., Khademi-Kalantari, K., Khalkhali-Zavieh, M., Rezasoltani, A., Ghasemi, M., Akbarzadeh Baghban, A., & Ghasemi, M. (2018). The Effect of Functional Stretching Exercises on Neural and Mechanical Properties of the Spastic Medial Gastrocnemius Muscle in Patients with Chronic Stroke: A Randomized Controlled Trial. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association, 27(7), 1733-1742. DOI: 10.1016/j.jstrokecerebrovasdis.2018.01.024.
Huang, T.H., Chou, L.W., Huang, C.Y., Wei, S.W., Tsai, Y.J., & Chen, Y.J. (2019). H-reflex in abductor hallucis and postural performance between flexible flatfoot and normal foot. Physical therapy in sport: official journal of the Association of Chartered Physiotherapists in Sports Medicine, 37, 27-33. DOI: 10.1016/j.ptsp.2019.02.004.
Unger, J., Andrushko, J.W., Oates, A.R., Renshaw, D.W., Barss, T.S., Zehr, E.P., & Farthing, J.P. (2019). Modulation of the Hoffmann reflex in the tibialis anterior with a change in posture. Physiological reports, 7(14), e14179. DOI: 10.14814/phy2.14179.
Melo, A.S.C., Taylor, J.L., Ferreira, R., Cunha, B., Ascenção, M., Fernandes, M., Sousa, V., Cruz, E.B., Vilas-Boas, J.P., & Sousa, A.S.P. (2023). Differences in Trapezius Muscle H-Reflex between Asymptomatic Subjects and Symptomatic Shoulder Pain Subjects. Sensors (Basel, Switzerland), 23(9), 4217. DOI: 10.3390/s23094217.
Libonati, L., Barone, T. F., Ceccanti, M., Cambieri, C., Tartaglia, G., Onesti, E., Petrucci, A., Frasca, V., & Inghilleri, M. (2019). Heteronymous H reflex in temporal muscle as sign of hyperexcitability in ALS patients. Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology, 130(8), 1455-1459. DOI: 0.1016/j.clinph. 2019.05.010.
Barss, T.S., Parhizi, B., Porter, J., & Mushahwar, V.K. (2022). Neural Substrates of Transcutaneous Spinal Cord Stimulation: Neuromodulation across Multiple Segments of the Spinal Cord. Journal of clinical medicine, 11(3), 639. DOI: 10.3390/jcm11030639.
Shen, H.Y., Lin, J.Y., Chen, C.C., Lee, H.F., Chao, H., Lieu, F.K., & Chen, S.F. (2022). Evaluation of post-stroke spasticity from the subacute to chronic stages: A clinical and neurophysiologic study of motoneuron pool excitability. The Chinese journal of physiology, 65(3), 109-116. DOI: 10.4103/0304-4920.348359.
Zhou, R., Parhizi, B., Assh, J., Alvarado, L., Ogilvie, R., Chong, S.L., & Mushahwar, V.K. (2018). Effect of cervicolumbar coupling on spinal reflexes during cycling after incomplete spinal cord injury. Journal of neurophysiology, 120(6), 3172-3186. DOI: 10.1152/jn.00509.2017.
Tøien, T., Unhjem, R., Øren, T.S., Kvellestad, A.C.G., Hoff, J., & Wang, E. (2018). Neural Plasticity with Age: Unilateral Maximal Strength Training Augments Efferent Neural Drive to the Contralateral Limb in Older Adults. The journals of gerontology. Series A, Biological sciences and medical sciences, 73(5), 596-602. DOI: 10.1093/gerona/glx218.
Hortobágyi, T., van de Waardt, L.E., Tokuno, C.D., Taube, W., & Papegaaij, S. (2018). Age-related reversal of spinal excitability during anticipatory postural control. European journal of applied physiology, 118(12), 2577-2585.
Johannsson, J., Duchateau, J., & Baudry, S. (2019). Modulation of the Hoffmann reflex in soleus and medial gastrocnemius during stair ascent and descent in young and older adults. Gait & posture, 68, 115-121. DOI: 10.1016/j.gaitpost.2018.11.018.
Škarabot, J., Ansdell, P., Brownstein, C.G., Hicks, K.M., Howatson, G., Goodall, S., & Durbaba, R. (2019). Reduced corticospinal responses in older compared with younger adults during submaximal isometric, shortening, and lengthening contractions. Journal of applied physiology (Bethesda, Md.: 1985), 126(4), 1015-1031. DOI: 10.1152/japplphysiol.00987.2018.
Lavender, A.P., Balkozak, S., Özyurt , M.G., Topkara, B., Karacan, İ., Bilici, İ., Hill, A.M., & Türker, K.S. (2020). Effect of aging on H-reflex response to fatigue.Exp Brain Res., 238(2), 273-282. DOI: 10.1007/s00221-019-05708-7.
Papavasileiou, A., Hatzitaki, V., Mademli, L., & Patikas, D.A. (2022). Temporal modulation of H-reflex in young and older people: Acute effects during Achilles tendon vibration while standing. Experimental gerontology, 165, 111844. DOI: 10.1016/j.exger.2022.111844.
Batista-Ferreira, L., Rabelo, N.F., da Cruz, G.M., Costa, J.N.A., Elias, L.A., & Mezzarane, R.A. (2022). Effects of voluntary contraction on the soleus H-reflex of different amplitudes in healthy young adults and in the elderly. Frontiers in human neuroscience, 16, 1039242. DOI: 10.3389/fnhum.2022.1039242.
Filho, S.S., Coelho, D.B., Ugrinowitsch, C., de Souza, C.R., Magalhães, F.H., de Lima-Pardini, A.C., de Oliveira, É.M.B., Mattos, E., Teixeira, L.A., & Silva-Batista, C. (2021). Age-Related Changes in Presynaptic Inhibition During Gait Initiation. The journals of gerontology. Series A, Biological sciences and medical sciences, 76(4), 568-575. DOI: 10.1093/gerona/glab010.
Mendonca, G.V., Pezarat-Correia, P., Gonçalves, A.D., Gomes, M., Correia, J.M., & Vila-Chã, C. (2020). Sex differences in soleus muscle H-reflex and V-wave excitability. Experimental physiology, 105(11), 1928-1938. DOI: 10.1113/EP088820.
Kinnunen, J.V., Piitulainen, H., & Piirainen, J.M. (2019). Neuromuscular Adaptations to Short-Term High-Intensity Interval Training in Female Ice-Hockey Players. Journal of strength and conditioning research, 33(2), 479-485. DOI: 10.1519/JSC.0000000000001881.
Stevanovic, V.B., Jelic, M.B., Milanovic, S.D., Filipovic, S.R., Mikic, M.J., & Stojanovic, M.D.M. (2019). Sport-Specific Warm-Up Attenuates Static Stretching- Induced Negative Effects on Vertical Jump But Not Neuromuscular Excitability in Basketball Players. Journal of sports science & medicine, 18(2), 282-289.
Tomazin, K., Almeida, F., Stirn, I., Padial, P., Bonitch-Góngora, J., Morales-Artacho, A.J., Strojnik, V., & Feriche, B. (2021). Neuromuscular Adaptations after an Altitude Training Camp in Elite Judo Athletes. International journal of environmental research and public health, 18(13), 6777. DOI: 10.3390/ijerph18136777.
Tomazin, K., Strojnik, V., Feriche, B., Garcia Ramos, A., Štrumbelj, B., & Stirn, I. (2022). Neuromuscular Adaptations in Elite Swimmers During Concurrent Strength and Endurance Training at Low and Moderate Altitudes. Journal of strength and conditioning research, 36(4), 1111-1119. DOI: 10.1519/JSC.0000000000003566.
Cecen, S., Niazi, I.K., Nedergaard, R.W., Cade, A., Allen, K., Holt, K., Haavik, H., & Türker, K.S. (2018). Posture modulates the sensitivity of the H-reflex. Experimental brain research, 236(3), 829-835. DOI: 10.1007/s00221-018-5182-x.
Hoque, M.M., Ardizzone, M.A., Sabatier, M., Borich, M.R., & Kesar, T.M. (2018). Longer Duration of Downslope Treadmill Walking Induces Depression of H-Reflexes Measured during Standing and Walking. Neurology (E-Cronicon), 10(8), 761-770. PMID: 31032493, PMCID: PMC6483108.
Lyle, M.A., McLeod, M.M., Pouliot, B.A., & Thompson, A.K. (2022). Soleus H-reflex modulation during a double-legged drop landing task. Experimental brain research, 240(4), 1093-1103. DOI: 10.1007/s00221-022-06316-8.
Ritzmann, R., Lee, K., Krause, A., Gollhofer, A., & Freyler, K. (2018). Stimulus Prediction and Postural Reaction: Phase-Specific Modulation of Soleus H-Reflexes Is Related to Changes in Joint Kinematics and Segmental Strategy in Perturbed Upright Stance. Frontiers in integrative neuroscience, 12, 62. DOI: 10.3389/fnint.2018.00062.
Miranda, Z., Pham, A., Elgbeili, G., &Barthélemy, D. (2019). H-reflex modulation preceding changes in soleus EMG activity during balance perturbation. Experimental brain research, 237(3), 777-791. DOI: 10.1007/s00221-018-5459-0.
Alizadehsaravi, L., Koster, R.A.J., Muijres, W., Maas, H., Bruijn, S.M., & van Dieën, J.H. (2022). The underlying mechanisms of improved balance after one and ten sessions of balance training in older adults. Human movement science, 81, 102910. DOI: 10.1016/j.humov.2021. 102910.
Matsuda, T., Kurayama, T., Tagami, M., Fujino, Y., Manji, A., Kusumoto, Y., & Amimoto, K. (2018). Influence of peripheral magnetic stimulation of soleus muscle on H and M waves. Journal of physical the rapyscience, 30(5), 716-718. DOI: 10.1589/jpts.30.716.
Alizadehsaravi, L., Bruijn, S.M., Maas, H., & van Dieën, J.H. (2020). Modulation of soleus muscle H-reflexes and ankle muscle co-contraction with surface compliance during unipedal balancing in young and older adults. Experimental brain research, 238(6), 1371-1383. DOI: 10.1007/s00221-020-05784-0.
Eftekhar, A., Norton, J.J.S., McDonough, C.M., & Wolpaw, J.R. (2018). Retraining Reflexes: Clinical Translation of Spinal Reflex Operant Conditioning. Neurotherapeutics: the journal of the American Society for Experimental NeuroTherapeutics, 15(3), 669-683. DOI: 10.1007/s13311-018-0643-2.
Phadke, C.P., Vierira, L., Mathur, S., Cipriano, G.Jr, Ismail, F., & Boulias, C. (2019). Impact of Passive Leg Cycling in Persons With Spinal Cord Injury: A Systematic Review. Topics in spinal cord injury rehabilitation, 25(1), 83-96. DOI: 10.1310/sci18-00020.
Fernandes, S.R., Pereira, M., Salvador, R., Miranda, P.C., & de Carvalho, M. (2019). Cervical trans-spinal direct current stimulation: a modelling-experimental approach. Journal of neuroengineering and rehabilitation, 16(1), 123. DOI: 10.1186/s12984-019-0589-6.
Yamaguchi, T., Beck, M.M., Therkildsen, E.R., Svane, C., Forman, C., Lorentzen, J., Conway, B.A., Lundbye-Jensen, J., Geertsen, S.S., & Nielsen, J.B. (2020). Transcutaneous spinal direct current stimulation increases corticospinal transmission and enhances voluntary motor output in humans. Physiological reports, 8(16), e14531. DOI: 10.14814/phy2.14531.
Traverse, E., Lebon, F., & Martin, A. (2018). Corticospinal and Spinal Excitabilities Are Modulated during Motor Imagery Associated with Somatosensory Electrical Nerve Stimulation. Neuralplasticity, 2018, 8265427. DOI: 10.1155/2018/8265427.
Kaneko, N., Masugi, Y., Usuda, N., Yokoyama, H., & Nakazawa, K. (2018). Modulation of Hoffmann reflex excitability during action observation of walking with and without motor imagery. Neuroscience letters, 684, 218-222. DOI: 10.1016/j.neulet.2018.07.041.
Keller, M., Taube, W., & Lauber, B. (2018). Task-dependent activation of distinct fast and slow(er) motor pathways during motor imagery. Brainstimulation, 11(4), 782–788. DOI: 10.1016/j.brs.2018.02.010.
Grosprêtre, S., Lebon, F., Papaxanthis, C., & Martin, A. (2019). Spinal plasticity with motor imagery practice. The Journal of physiology, 597(3), 921-934. DOI: 10.1113/JP276694.
Cattagni, T., Merlet, A.N., Cornu, C., & Jubeau, M. (2018). H-reflex and M-wave recordings: effect of pressure application to the stimulation electrode on the assessment of evoked potentials and subject’s discomfort. Clinical physiology and functional imaging, 38(3), 416-424. DOI: 10.1111/cpf.12431.
Piponnier, E., Ratel, S., François, B., Garcia-Vicencio, S., & Martin, V. (2018). Assessment of the H-reflex using two synchronized magnetic stimulators in order to increase stimulus durations: A comparison with electrical stimulation. Neuroscience letters, 675, 89-94. DOI: 10.1016/j.neulet.2018.03.039.
Özyurt, M.G., Shabsog, M., Dursun, M., & Türker, K.S. (2018). Optimal location for eliciting the tibial H-reflex and motor response. Muscle & nerve, 58(6), 828-833. DOI: 10.1002/mus.26308.
Lewis, M.J., Laber, E., & Olby, N.J. (2019). Predictors of Response to 4-Aminopyridine in Chronic Canine Spinal Cord Injury. Journal of neurotrauma, 36(9), 1428-1434. DOI: 10.1089/neu.2018.5975.
Synowiec, S., Lu, J., Yu, L., Goussakov, I., Lieber, R., & Drobyshevsky, A. (2019). Spinal Hyper-Excitability and Altered Muscle Structure Contribute to Muscle Hypertonia in Newborns After Antenatal Hypoxia-Ischemia in a Rabbit Cerebral Palsy Model. Frontiers in neurology, 9, 1183. DOI: 10.3389/fneur.2018.01183.
Nielsen, J.B., Morita, H., Wenzelburger, R., Deuschl, G., Gossard, J.P., & Hultborn, H. (2019). Recruitment gain of spinal motor neuron pools in cat and human. Experimental brain research, 237(11), 2897-2909. DOI: 10.1007/s00221-019-05628-6.
Jeffrey-Gauthier, R., Piché, M., &Leblond, H. (2019). H-reflex disinhibition by lumbar muscle inflammation in a mouse model of spinal cord injury. Neuroscience letters, 690, 36-41. DOI: 10.1016/j.neulet.2018.10.005.
Gong, C., Zheng, X., Guo, F., Wang, Y., Zhang, S., Chen, J., Sun, X., …, & Chen, H. (2021). Human spinal GABA neurons alleviate spasticity and improve locomotion in rats with spinal cord injury. Cell reports, 34(12), 108889. DOI: 10.1016/j.celrep.2021.108889.
Wieters, F., Weiss Lucas, C., Gruhn, M., Büschges, A., Fink, G.R., & Aswendt, M. (2021). Introduction to spasticity and related mouse models. Experimental neurology, 335, 113491. DOI: 10.1016/j.expneurol.2020.113491.
Benson, C.A., Olson, K.L., Patwa, S., Reimer, M.L., Bangalore, L., Hill, M., Waxman, S.G., & Tan, A.M. (2021). Conditional RAC1 knockout in motor neurons restores H-reflex rate-dependent depression after spinal cord injury. Scientific reports, 11(1), 7838. DOI: 10.1038/s41598-021-87476-5.
Cordero, K., Coronel, G.G., Serrano-Illán, M., Cruz-Bracero, J., Figueroa, J.D., & De León, M. (2018). Effects of Dietary Vitamin E Supplementation in Bladder Function and Spasticity during Spinal Cord Injury. Brain sciences, 8(3), 38. DOI: 10.3390/brainsci8030038.
