دورية أكاديمية
Muscle contractile properties directly influence shared synaptic inputs to spinal motor neurons.
العنوان: | Muscle contractile properties directly influence shared synaptic inputs to spinal motor neurons. |
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المؤلفون: | Cabral HV; Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy., Inglis JG; Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy., Cudicio A; Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy., Cogliati M; Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy., Orizio C; Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy., Yavuz US; Biomedical Signals and Systems, University of Twente, Enschede, Netherlands., Negro F; Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy. |
المصدر: | The Journal of physiology [J Physiol] 2024 Jun; Vol. 602 (12), pp. 2855-2872. Date of Electronic Publication: 2024 May 06. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Cambridge Univ. Press Country of Publication: England NLM ID: 0266262 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-7793 (Electronic) Linking ISSN: 00223751 NLM ISO Abbreviation: J Physiol Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Oxford : Blackwell : Cambridge Univ. Press Original Publication: London, Cambridge Univ. Press. |
مواضيع طبية MeSH: | Motor Neurons*/physiology , Muscle, Skeletal*/physiology , Muscle, Skeletal*/innervation , Muscle Contraction*/physiology, Humans ; Male ; Adult ; Female ; Electromyography ; Young Adult ; Synapses/physiology ; Spinal Cord/physiology |
مستخلص: | Alpha band oscillations in shared synaptic inputs to the alpha motor neuron pool can be considered an involuntary source of noise that hinders precise voluntary force production. This study investigated the impact of changing muscle length on the shared synaptic oscillations to spinal motor neurons, particularly in the physiological tremor band. Fourteen healthy individuals performed low-level dorsiflexion contractions at ankle joint angles of 90° and 130°, while high-density surface electromyography (HDsEMG) was recorded from the tibialis anterior (TA). We decomposed the HDsEMG into motor units spike trains and calculated the motor units' coherence within the delta (1-5 Hz), alpha (5-15 Hz), and beta (15-35 Hz) bands. Additionally, force steadiness and force spectral power within the tremor band were quantified. Results showed no significant differences in force steadiness between 90° and 130°. In contrast, alpha band oscillations in both synaptic inputs and force output decreased as the length of the TA was moved from shorter (90°) to longer (130°), with no changes in delta and beta bands. In a second set of experiments (10 participants), evoked twitches were recorded with the ankle joint at 90° and 130°, revealing longer twitch durations in the longer TA muscle length condition compared to the shorter. These experimental results, supported by a simple computational simulation, suggest that increasing muscle length enhances the muscle's low-pass filtering properties, influencing the oscillations generated by the Ia afferent feedback loop. Therefore, this study provides valuable insights into the interplay between muscle biomechanics and neural oscillations. KEY POINTS: We investigated whether changes in muscle length, achieved by changing joint position, could influence common synaptic oscillations to spinal motor neurons, particularly in the tremor band (5-15 Hz). Our results demonstrate that changing muscle length from shorter to longer induces reductions in the magnitude of alpha band oscillations in common synaptic inputs. Importantly, these reductions were reflected in the oscillations of muscle force output within the alpha band. Longer twitch durations were observed in the longer muscle length condition compared to the shorter, suggesting that increasing muscle length enhances the muscle's low-pass filtering properties. Changes in the peripheral contractile properties of motor units due to changes in muscle length significantly influence the transmission of shared synaptic inputs into muscle force output. These findings prove the interplay between muscle mechanics and neural adaptations. (© 2024 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.) |
References: | Baker, S. N., Olivier, E., & Lemon, R. N. (1997). Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation. The Journal of Physiology, 501(Pt 1), 225–241. Baker, S. N., Pinches, E. M., & Lemon, R. N. (2003). Synchronization in monkey motor cortex during a precision grip task. II. effect of oscillatory activity on corticospinal output. Journal of Neurophysiology, 89(4), 1941–1953. Baldissera, F., Cavallari, P., & Cerri, G. (1998). Motoneuronal pre‐compensation for the low‐pass filter characteristics of muscle. A quantitative appraisal in cat muscle units. The Journal of Physiology, 511(Pt 2), 611–627. Bawa, P., & Stein, R. B. (1976). Frequency response of human soleus muscle. Journal of Neurophysiology, 39(4), 788–793. Berniker, M., Jarc, A., Bizzi, E., & Tresch, M. C. (2009). Simplified and effective motor control based on muscle synergies to exploit musculoskeletal dynamics. Proceedings of the National Academy of Sciences, USA, 106(18), 7601–7606. Bigland‐Ritchie, B. R., Furbush, F. H., Gandevia, S. C., & Thomas, C. K. (1992). Voluntary discharge frequencies of human motoneurons at different muscle lengths. Muscle & Nerve, 15(2), 130–137. Bräcklein, M., Barsakcioglu, D. Y., Del Vecchio, A., Ibáñez, J., & Farina, D. (2022). Reading and modulating cortical β bursts from motor unit spiking activity. The Journal of Neuroscience, 42(17), 3611–3621. Bremner, F. D., Baker, J. R., & Stephens, J. A. (1991). Correlation between the discharges of motor units recorded from the same and from different finger muscles in man. The Journal of Physiology, 432(1), 355–380. Castronovo, A. M., Negro, F., Conforto, S., & Farina, D. (2015). The proportion of common synaptic input to motor neurons increases with an increase in net excitatory input. Journal of Applied Physiology, 119(11), 1337–1346. Castronovo, A. M., Negro, F., & Farina, D. (2015). Theoretical model and experimental validation of the estimated proportions of common and independent input to motor neurons. Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2015, 254–257. Christakos, C. N., Papadimitriou, N. A., & Erimaki, S. (2006). Parallel neuronal mechanisms underlying physiological force tremor in steady muscle contractions of humans. Journal of Neurophysiology, 95(1), 53–66. Clamann, H. P., & Schelhorn, T. B. (1988). Nonlinear force addition of newly recruited motor units in the cat hindlimb. Muscle & Nerve, 11, 1079–1089. Cogliati, M., Cudicio, A., Martinez‐Valdes, E., Tarperi, C., Schena, F., Orizio, C., & Negro, F. (2020). Half marathon induces changes in central control and peripheral properties of individual motor units in master athletes. Journal of Electromyography and Kinesiology, 55, 102472. Conway, B. A., Halliday, D. M., Farmer, S. F., Shahani, U., Maas, P., Weir, A. I., & Rosenberg, J. R. (1995). Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. The Journal of Physiology, 489(Pt 3), 917–924. Cresswell, A. G., & Löscher, W. N. (2000). Significance of peripheral afferent input to the alpha‐motoneurone pool for enhancement of tremor during an isometric fatiguing contraction. European Journal of Applied Physiology, 82(1–2), 129–136. Cudicio, A., Martinez‐Valdes, E., Cogliati, M., Orizio, C., & Negro, F. (2022). The force‐generation capacity of the tibialis anterior muscle at different muscle‐tendon lengths depends on its motor unit contractile properties. European Journal of Applied Physiology, 122(2), 317–330. D'avella, A., & Bizzi, E. (2005). Shared and specific muscle synergies in natural motor behaviors. Proceedings of the National Academy of Sciences, USA, 102(8), 3076–3081. Datta, A. K., Farmer, S. F., & Stephens, J. A. (1991). Central nervous pathways underlying synchronization of human motor unit firing studied during voluntary contractions. The Journal of Physiology, 432(1), 401–425. Datta, A. K., & Stephens, J. A. (1990). Synchronization of motor unit activity during voluntary contraction in man. The Journal of Physiology, 422(1), 397–419. De Luca, C. J., Gonzalez‐Cueto, J. A., Bonato, P., & Adam, A. (2009). Motor unit recruitment and proprioceptive feedback decrease the common drive. Journal of Neurophysiology, 101(3), 1620–1628. De Luca, C. J., Lefever, R. S., Mccue, M. P., & Xenakis, A. P. (1982). Control scheme governing concurrently active human motor units during voluntary contractions. The Journal of Physiology, 329(1), 129–142. Dideriksen, J., Elias, L. A., Zambalde, E. P., Germer, C. M., Molinari, R. G., & Negro, F. (2022). Influence of central and peripheral motor unit properties on isometric muscle force entropy: A computer simulation study. Journal of Biomechanics, 139, 110866. Dideriksen, J. L., & Negro, F. (2018). Spike‐triggered averaging provides inaccurate estimates of motor unit twitch properties under optimal conditions. Journal of Electromyography and Kinesiology, 43, 104–110. Dideriksen, J. L., Negro, F., Enoka, R. M., & Farina, D. (2012). Motor unit recruitment strategies and muscle properties determine the influence of synaptic noise on force steadiness. Journal of Neurophysiology, 107(12), 3357–3369. Duchateau, J., & Enoka, R. M. (2011). Human motor unit recordings: Origins and insight into the integrated motor system. Brain Research, 1409, 42–61. Enoka, R. M., Christou, E. A., Hunter, S. K., Kornatz, K. W., Semmler, J. G., Taylor, A. M., & Tracy, B. L. (2003). Mechanisms that contribute to differences in motor performance between young and old adults. Journal of Electromyography and Kinesiology, 13(1), 1–12. Enoka, R. M., & Farina, D. (2021). Force steadiness: From motor units to voluntary actions. Physiology (Bethesda, Md.), 36, 114–130. Farina, D., & Negro, F. (2015). Common synaptic input to motor neurons, motor unit synchronization, and force control. Exercise and Sport Sciences Reviews, 43(1), 23–33. Farina, D., Negro, F., & Dideriksen, J. L. (2014). The effective neural drive to muscles is the common synaptic input to motor neurons. The Journal of Physiology, 592(16), 3427–3441. Farmer, S. F., Bremner, F. D., Halliday, D. M., Rosenberg, J. R., & Stephens, J. A. (1993). The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. The Journal of Physiology, 470(1), 127–155. Feeney, D. F., Mani, D., & Enoka, R. M. (2018). Variability in common synaptic input to motor neurons modulates both force steadiness and pegboard time in young and older adults. The Journal of Physiology, 596(16), 3793–3806. Feinstein, B., Lindegård, B., Nyman, E., & Wohlfart, G. (1955). Morphologic studies of motor units in normal human muscles. Acta Anatomica, 23(2), 127–142. Fuglevand, A. J., Winter, D. A., & Patla, A. E. (1993). Models of recruitment and rate coding organization in motor‐unit pools. Journal of Neurophysiology, 70(6), 2470–2488. Gallet, C., & Julien, C. (2011). The significance threshold for coherence when using the Welch's periodogram method: Effect of overlapping segments. Biomedical Signal Processing and Control, 6(4), 405–409. Gogeascoechea, A., Ornelas‐Kobayashi, R., Yavuz, U. S., & Sartori, M. (2023). Characterization of motor unit firing and twitch properties for decoding musculoskeletal force in the human ankle joint in vivo. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 31, 4040–4050. Hagbarth, K.‐E., & Young, R. R. (1979). Participation of the stretch reflex in human physiological tremor. Brain, 102(3), 509–526. Halliday, A. M., & Redfearn, J. W. T. (1956). An analysis of the frequencies of finger tremor in healthy subjects. The Journal of Physiology, 134(3), 600–611. Hassan, A., Thompson, C. K., Negro, F., Cummings, M., Powers, R. K., Heckman, C. J., Dewald, J. P. A., & Mcpherson, L. M. (2020). Impact of parameter selection on estimates of motoneuron excitability using paired motor unit analysis. Journal of Neural Engineering, 17(1), 016063. Heckman, C. J., & Enoka, R. M. (2012). Motor unit. Comprehensive Physiology, 2, 2629–2682. Henderson, T. T., Thorstensen, J. R., Morrison, S., Tucker, M. G., & Kavanagh, J. J. (2022). Physiological tremor is suppressed and force steadiness is enhanced with increased availability of serotonin regardless of muscle fatigue. Journal of Neurophysiology, 127(1), 27–37. Hug, F., Avrillon, S., Del Vecchio, A., Casolo, A., Ibanez, J., Nuccio, S., Rossato, J., Holobar, A., & Farina, D. (2021). Analysis of motor unit spike trains estimated from high‐density surface electromyography is highly reliable across operators. Journal of Electromyography and Kinesiology, 58, 102548. Hug, F., Avrillon, S., Ibáñez, J., & Farina, D. (2023). Common synaptic input, synergies and size principle: Control of spinal motor neurons for movement generation. The Journal of Physiology, 601(1), 11–20. Inglis, J. G., & Gabriel, D. A. (2021). Sex differences in the modulation of the motor unit discharge rate leads to reduced force steadiness. Applied Physiology, Nutrition and Metabolism, 46(9), 1065–1072. Ishizuka, N., Mannen, H., Hongo, T., & Sasaki, S. (1979). Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: Three dimensional reconstructions from serial sections. Journal of Comparative Neurology, 186(2), 189–211. Jalaleddini, K., Nagamori, A., Laine, C. M., Golkar, M. A., Kearney, R. E., & Valero‐Cuevas, F. J. (2017). Physiological tremor increases when skeletal muscle is shortened: Implications for fusimotor control. The Journal of Physiology, 595(24), 7331–7346. Kaneda, K., Wakabayashi, H., Sato, D., Uekusa, T., & Nomura, T. (2008). Lower extremity muscle activity during deep‐water running on self‐determined pace. Journal of Electromyography and Kinesiology, 18(6), 965–972. Kerkman, J. N., Daffertshofer, A., Gollo, L. L., Breakspear, M., & Boonstra, T. W. (2018). Network structure of the human musculoskeletal system shapes neural interactions on multiple time scales. Science Advances, 4(6), eaat0497. Kirkwood, P. A., & Sears, T. A. (1978). The synaptic connexions to intercostal motoneurones as revealed by the average common excitation potential. The Journal of Physiology, 275(1), 103–134. Koželj, S., & Baker, S. N. (2014). Different phase delays of peripheral input to primate motor cortex and spinal cord promote cancellation at physiological tremor frequencies. Journal of Neurophysiology, 111(10), 2001–2016. Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1–26. Laine, C. M., Martinez‐Valdes, E., Falla, D., Mayer, F., & Farina, D. (2015). Motor neuron pools of synergistic thigh muscles share most of their synaptic input. The Journal of Neuroscience, 35(35), 12207–12216. Laine, C. M., Nagamori, A., & Valero‐Cuevas, F. J. (2016). The dynamics of voluntary force production in afferented muscle influence involuntary tremor. Frontiers in Computational Neuroscience, 10, 86. Laine, C. M., Yavuz, Ş. U., & Farina, D. (2014). Task‐related changes in sensorimotor integration influence the common synaptic input to motor neurones. Acta Physiology, 211(1), 229–239. Lemon, R. N. (2008). Descending pathways in motor control. Annual Review of Neuroscience, 31(1), 195–218. Lenth, R., Singmann, H., Love, J., Buerkner, P., & Herve, M. (2019). Package ‘emmeans’. Lippold, O. (1971). Physiological tremor. Scientific American, 224(3), 65–73. Lippold, O. C. J. (1970). Oscillation in the stretch reflex arc and the origin of the rhythmical, 8–12 C‐S component of physiological tremor. The Journal of Physiology, 206(2), 359–382. Mannard, A., & Stein, R. B. (1973). Determination of the frequency response of isometric soleus muscle in the cat using random nerve stimulation. The Journal of Physiology, 229(2), 275–296. Marsh, E., Sale, D., Mccomas, A. J., & Quinlan, J. (1981). Influence of joint position on ankle dorsiflexion in humans. Journal of Applied Physiology, 51(1), 160–167. Martinez‐Valdes, E., Negro, F., Laine, C. M., Falla, D., Mayer, F., & Farina, D. (2017). Tracking motor units longitudinally across experimental sessions with high‐density surface electromyography. The Journal of Physiology, 595(5), 1479–1496. Mcauley, J. H. (2000). Physiological and pathological tremors and rhythmic central motor control. Brain, 123(Pt 8), 1545–1567. Mcmanus, L., Flood, M. W., & Lowery, M. M. (2019). Beta‐band motor unit coherence and nonlinear surface EMG features of the first dorsal interosseous muscle vary with force. Journal of Neurophysiology, 122(3), 1147–1162. Mela, P., Veltink, P. H., & Huijing, P. A. (2001). The influence of stimulation frequency and ankle joint angle on the moment exerted by human dorsiflexor muscles. Journal of Electromyography and Kinesiology, 11(1), 53–63. Mitchell, B., Bressel, E., Mcnair, P. J., & Bressel, M. E. (2008). Effect of pelvic, hip, and knee position on ankle joint range of motion. Physical Therapy in Sport, 9(4), 202–208. Muceli, S., Poppendieck, W., Holobar, A., Gandevia, S., Liebetanz, D., & Farina, D. (2022). Blind identification of the spinal cord output in humans with high‐density electrode arrays implanted in muscles. Science Advances, 8(46), eabo5040. Negro, F., & Farina, D. (2011). Linear transmission of cortical oscillations to the neural drive to muscles is mediated by common projections to populations of motoneurons in humans. The Journal of Physiology, 589(3), 629–637. Negro, F., & Farina, D. (2012). Factors influencing the estimates of correlation between motor unit activities in humans. PLoS ONE, 7(9), e44894. Negro, F., Holobar, A., & Farina, D. (2009). Fluctuations in isometric muscle force can be described by one linear projection of low‐frequency components of motor unit discharge rates. The Journal of Physiology, 587(24), 5925–5938. Negro, F., Muceli, S., Castronovo, A. M., Holobar, A., & Farina, D. (2016). Multi‐channel intramuscular and surface EMG decomposition by convolutive blind source separation. Journal of Neural Engineering, 13(2), 026027. Ng, A. V., Agre, J. C., Hanson, P., Harrington, M. S., & Nagle, F. J. (1994). Influence of muscle length and force on endurance and pressor responses to isometric exercise. Journal of Applied Physiology, 76(6), 2561–2569. Nordstrom, M. A., Fuglevand, A. J., & Enoka, R. M. (1992). Estimating the strength of common input to human motoneurons from the cross‐correlogram. The Journal of Physiology, 453(1), 547–574. Pääsuke, M., Ereline, J., & Gapeyeva, H. (2001). Knee extension strength and vertical jumping performance in nordic combined athletes. Journal of Sports Medicine and Physical Fitness, 41, 354–361. Petrovic, I., Amiridis, I. G., Holobar, A., Trypidakis, G., Kellis, E., & Enoka, R. M. (2022). Leg dominance does not influence maximal force, force steadiness, or motor unit discharge characteristics. Medicine & Science in Sports & Exercise, 54. Powers, R. K., & Binder, M. D. (1991). Effects of low‐frequency stimulation on the tension‐frequency relations of fast‐twitch motor units in the cat. Journal of Neurophysiology, 66(3), 905–918. Rack, P. M. H., & Westbury, D. R. (1969). The effects of length and stimulus rate on tension in the isometric cat soleus muscle. The Journal of Physiology, 204(2), 443–460. Rossato, J., Tucker, K., Avrillon, S., Lacourpaille, L., Holobar, A., & Hug, F. (2022). Less common synaptic input between muscles from the same group allows for more flexible coordination strategies during a fatiguing task. Journal of Neurophysiology, 127(2), 421–433. Sears, T. A., & Stagg, D. (1976). Short‐term synchronization of intercostal motoneurone activity. The Journal of Physiology, 263(3), 357–381. Taylor, A. M., Steege, J. W., & Enoka, R. M. (2002). Motor‐unit synchronization alters spike‐triggered average force in simulated contractions. Journal of Neurophysiology, 88(1), 265–276. Thompson, C. K., Negro, F., Johnson, M. D., Holmes, M. R., Mcpherson, L. M., Powers, R. K., Farina, D., & Heckman, C. J. (2018). Robust and accurate decoding of motoneuron behaviour and prediction of the resulting force output. The Journal of Physiology, 596(14), 2643–2659. Tsatsaki, E., Amiridis, I. G., Holobar, A., Trypidakis, G., Arabatzi, F., Kellis, E., & Enoka, R. M. (2022). The length of tibialis anterior does not influence force steadiness during submaximal isometric contractions with the dorsiflexors. European Journal of Sport Science, 22(4), 539–548. Williams, E. R., Soteropoulos, D. S., & Baker, S. N. (2010). Spinal interneuron circuits reduce approximately 10‐Hz movement discontinuities by phase cancellation. Proceedings of the National Academy of Sciences, 107(24), 11098–11103. Wu, R., Delahunt, E., Ditroilo, M., Lowery, M. M., Segurado, R., & De Vito, G. (2019). Changes in knee joint angle affect torque steadiness differently in young and older individuals. Journal of Electromyography and Kinesiology, 47, 49–56. Yao, W., Fuglevand, R. J., & Enoka, R. M. (2000). Motor‐unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. Journal of Neurophysiology, 83(1), 441–452. Yavuz, Ş. U., Şendemir‐Ürkmez, A., & Türker, K. S. (2010). Effect of gender, age, fatigue and contraction level on electromechanical delay. Clinical Neurophysiology, 121(10), 1700–1706. Yavuz, U. Ş., Negro, F., Diedrichs, R., & Farina, D. (2018). Reciprocal inhibition between motor neurons of the tibialis anterior and triceps surae in humans. Journal of Neurophysiology, 119(5), 1699–1706. Yavuz, U. Ş., Negro, F., Falla, D., & Farina, D. (2015). Experimental muscle pain increases variability of neural drive to muscle and decreases motor unit coherence in tremor frequency band. Journal of Neurophysiology, 114(2), 1041–1047. |
معلومات مُعتمدة: | 101045605 HORIZON EUROPE European Research Council |
فهرسة مساهمة: | Keywords: common synaptic input; force control; motor unit; muscle mechanics; twitch force |
تواريخ الأحداث: | Date Created: 20240506 Date Completed: 20240614 Latest Revision: 20240614 |
رمز التحديث: | 20240614 |
DOI: | 10.1113/JP286078 |
PMID: | 38709959 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1469-7793 |
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DOI: | 10.1113/JP286078 |