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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/10.1016/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/10.1007/s00421-018-3982-0
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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/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. DOI: https://doi.org/10.3390/brainsci8030038
