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Remote muscle contraction enhances spinal reflexes in multiple lower-limb muscles elicited by transcutaneous spinal cord stimulation

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Abstract

Transcutaneous spinal cord stimulation (tSCS) is a useful technique for the clinical assessment of neurological disorders. However, the characteristics of the spinal cord circuits activated by tSCS are not yet fully understood. In this study, we examined whether remote muscle contraction enhances the spinal reflexes evoked by tSCS in multiple lower-limb muscles. Eight healthy men participated in the current experiment, which required them to grip a dynamometer as fast as possible after the presentation of an auditory cue. Spinal reflexes were evoked in multiple lower-limb muscles with different time intervals (50–400 ms) after the auditory signals. The amplitudes of the spinal reflexes in all the recorded leg muscles significantly increased at 50–250 ms after remote muscle activation onset. This suggests that remote muscle contraction simultaneously facilitates the spinal reflexes in multiple lower-limb muscles. In addition, eight healthy men performed five different tasks (i.e., rest, hand grip, pinch grip, elbow flexion, and shoulder flexion). Compared to control values recorded just before each task, the spinal reflexes evoked at 250 ms after the auditory signals were significantly enhanced by the above tasks except for the rest task. This indicates that such facilitatory effects are also induced by remote muscle contractions in different upper-limb areas. The present results demonstrate the existence of a neural interaction between remote upper-limb muscles and spinal reflex circuits activated by tSCS in multiple lower-limb muscles. The combination of tSCS and remote muscle contraction may be useful for the neurological examination of spinal cord circuits.

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Abbreviations

APB:

Abductor pollicis brevis

AD:

Anterior deltoid

BB:

Biceps brachii

BF:

Biceps femoris

EMG:

Electromyographic

Exp:

Experiment

ECR:

Extensor carpi radialis

FDI:

First dorsal interosseous

FCR:

Flexor carpi radialis

H-reflex:

Hoffmann reflex

JM:

Jendrássik maneuver

MVC:

Maximum voluntary contraction

MVF:

Maximum voluntary force

MG:

Medial gastrocnemius

RMS:

Root mean square

SOL:

Soleus

T-reflex:

Tendon-reflex

TA:

Tibialis anterior

tSCS:

Transcutaneous spinal cord stimulation

VM:

Vastus medialis

References

  • Andriyanova EY (2010) Characteristics of multisegmental monosynaptic responses of leg muscles in subjects with lumber nerve compression. Hum Physiol 36:440–446

    Article  Google Scholar 

  • Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG (2000) Voluntary teeth clenching facilitates human motor system excitability. Clin Neurophysiol 111:988–993

    Article  CAS  PubMed  Google Scholar 

  • Burke JR, Schutten MC, Koceja DM, Kamen G (1996) Age-dependent effects of muscle vibration and the Jendrassik maneuver on the patellar tendon reflex response. Arch Phys Med Rehabil 77:600–604

    Article  CAS  PubMed  Google Scholar 

  • Bussel B, Morin C, Pierrot-Deseilligny E (1978) Mechanism of monosynaptic reflex reinforcement during Jendrassik manoeuvre in man. J Neurol Neurosurg Psychiatry 41:40–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Courtine G, Harkema SJ, Dy CJ, Gerasimenko YP, Dyhre-Poulsen P (2007) Modulation of multisegmental monosynaptic responses in a variety of leg muscles during walking and running in humans. J Physiol 582:1125–1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danner SM, Hofstoetter US, Ladenbauer J, Rattay F, Minassian K (2011) Can the human lumbar posterior columns be stimulated by transcutaneous spinal cord stimulation? A modeling study. Artif Organs 35:257–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Danner SM, Krenn M, Hofstoetter US, Toth A, Mayr W, Minassian K (2016) Body position influences which neural structures are recruited by lumbar transcutaneous spinal cord stimulation. PLoS One 11:e0147479

    Article  PubMed  PubMed Central  Google Scholar 

  • Delwaide PJ, Toulouse P (1980) Jendrassik maneuver vs controlled contractions conditioning the excitability of soleus monosynaptic reflexes. Arch Phys Med Rehabil 61:505–510

    CAS  PubMed  Google Scholar 

  • Delwaide PJ, Toulouse P (1981) Facilitation of monosynaptic reflexes by voluntary contraction of muscle in remote parts of the body. Mechanisms involved in the Jendrassik Manoeuvre. Brain 104:701–709

    Article  CAS  PubMed  Google Scholar 

  • Dietz V, Muller R, Colombo G (2002) Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 125:2626–2634

    Article  PubMed  Google Scholar 

  • Dowman R, Wolpaw JR (1988) Jendrassik maneuver facilitates soleus H-reflex without change in average soleus motoneuron pool membrane potential. Exp Neurol 101:288–302

    Article  CAS  PubMed  Google Scholar 

  • Dy CJ, Gerasimenko YP, Edgerton VR, Dyhre-Poulsen P, Courtine G, Harkema SJ (2010) Phase-dependent modulation of percutaneously elicited multisegmental muscle responses after spinal cord injury. J Neurophysiol 103:2808–2820

    Article  PubMed  PubMed Central  Google Scholar 

  • Furubayashi T, Sugawara K, Kasai T, Hayashi A, Hanajima R, Shiio Y, Iwata NK, Ugawa Y (2003) Remote effects of self-paced teeth clenching on the excitability of hand motor area. Exp Brain Res 148:261–265

    Article  PubMed  Google Scholar 

  • Gerasimenko YP, Lu DC, Modaber M, Zdunowski S, Gad P, Sayenko DG, Morikawa E, Haakana P, Ferguson AR, Roy RR, Edgerton VR (2015) Noninvasive reactivation of motor descending control after paralysis. J Neurotrauma 32:1968–1980

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagbarth KE, Wallin G, Burke D, Löfstedt L (1975) Effects of the Jendrassik manoeuvre on muscle spindle activity in man. J Neurol Neurosurg Psychiatry 38:1143–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubli M, Dietz V (2013) The physiological basis of neurorehabilitation-locomotor training after spinal cord injury. J Neuroeng Rehabil 10:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawamura T, Watanabe S (1975) Timing as a prominent factor of the Jendrassik manoeuvre on the H reflex. J Neurol Neurosurg Psychiatry 38:508–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitano K, Koceja DM (2009) Spinal reflex in human lower leg muscles evoked by transcutaneous spinal cord stimulation. J Neurosci Methods 180:111–115

    Article  PubMed  Google Scholar 

  • Kojima N, Nakazawa K, Yamamoto S-I, Yano H (1998) Phase-dependent electromyographic activity of the lower-limb muscles of a patient with clinically complete spinal cord injury during orthotic gait. Exp Brain Res 120:139–142

    Article  CAS  PubMed  Google Scholar 

  • Kojima N, Nakazawa K, Yano H (1999) Effects of limb loading on the lower-limb electromyographic activity during orthotic locomotion in a paraplegic patient. Neurosci Lett 274:211–213

    Article  CAS  PubMed  Google Scholar 

  • Krenn M, Hofstoetter US, Danner SM, Minassian K, Mayr W (2015) Multi-electrode array for transcutaneous lumbar posterior root stimulation. Artif Organs 39:834–840

    Article  PubMed  Google Scholar 

  • Landau WM, Clare MH (1964) Fusimotor function. VI. H reflex, tendon jerk, and reinforcement in hemiplegia. Arch Neurol 10:128–134

    Article  CAS  PubMed  Google Scholar 

  • Masugi Y, Obata H, Nakazawa K (2017) Effects of anode position on the responses elicited by transcutaneous spinal cord stimulation. Conf Proc IEEE Eng Med Biol Soc 2017:1114–1117

    PubMed  Google Scholar 

  • Minassian K, Persy I, Rattay F, Dimitrijevic MR, Hofer C, Kern H (2007) Posterior root-muscle reflexes elicited by transcutaneous stimulation of the human lumbosacral cord. Muscle Nerve 35:327–336

    Article  PubMed  Google Scholar 

  • Miyahara T, Hagiya N, Ohyama T, Nakamura Y (1996) Modulation of human soleus H reflex in association with voluntary clenching of the teeth. J Neurophysiol 76:2033–2041

    Article  CAS  PubMed  Google Scholar 

  • Roy FD, Gibson G, Stein RB (2012) Effect of percutaneous stimulation at different spinal levels on the activation of sensory and motor roots. Exp Brain Res 223:281–289

    Article  PubMed  Google Scholar 

  • Roy FD, Bosgra D, Stein RB (2014) Interaction of transcutaneous spinal stimulation and transcranial magnetic stimulation in human leg muscles. Exp Brain Res 232:1717–1728

    Article  PubMed  Google Scholar 

  • Sayenko DG, Atkinson DA, Dy CJ, Gurley KM, Smith VL, Angeli C, Harkema SJ, Edgerton VR, Gerasimenko YP (2015) Spinal segment-specific transcutaneous stimulation differentially shapes activation pattern among motor pools in humans. J Appl Physiol (1985) 118:1364–1374

    Article  PubMed Central  Google Scholar 

  • Sugawara K, Kasai T (2002) Facilitation of motor evoked potentials and H-reflexes of flexor carpi radialis muscle induced by voluntary teeth clenching. Hum Mov Sci 21:203–212

    Article  PubMed  Google Scholar 

  • Takada Y, Miyahara T, Tanaka T, Ohyama T, Nakamura Y (2000) Modulation of H reflex of pretibial muscles and reciprocal Ia inhibition of soleus muscle during voluntary teeth clenching in humans. J Neurophysiol 83:2063–2070

    Article  CAS  PubMed  Google Scholar 

  • Takeoka A, Vollenweider I, Courtine G, Arber S (2014) Muscle spindle feedback directs locomotor recovery and circuit reorganization after spinal cord injury. Cell 159:1626–1639

    Article  CAS  PubMed  Google Scholar 

  • Tazoe T, Komiyama T (2014) Interlimb neural interactions in the corticospinal pathways. J Sports Med Phys Fit 3:181–190

    Article  Google Scholar 

  • Tazoe T, Kida T, Wasaka T, Sakamoto M, Nakajima T, Nishihira Y, Komiyama T (2005) Attenuation of the effect of remote muscle contraction on the soleus H-reflex during plantar flexion. Clin Neurophysiol 116:1362–1369

    Article  CAS  PubMed  Google Scholar 

  • Troni W, Di Sapio A, Berra E, Duca S, Merola A, Sperli F, Bertolotto A (2011) A methodological reappraisal of non invasive high voltage electrical stimulation of lumbosacral nerve roots. Clin Neurophysiol 122:2071–2080

    Article  PubMed  Google Scholar 

  • Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468

    Article  PubMed  Google Scholar 

  • Zehr EP, Stein RB (1999) Interaction of the Jendrassik maneuver with segmental presynaptic inhibition. Exp Brain Res 124:474–480

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by JSPS KAKENHI Grant number 18K17760.

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Correspondence to Kimitaka Nakazawa.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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221_2019_5536_MOESM1_ESM.tif

Supplementary Fig.1: Results of the double-pulse stimulation test: A) Typical example of the averaged waveform of the responses elicited by double-pulse stimulation (n=1) in multiple lower-limb muscles. tSCS was delivered at 0 ms and 50 ms. B) Medians (n=8) of the peak to-peak amplitude of both the first and the second response. The lines in the box plots indicate the medians. The ends of the boxes represent the 25th and 75th percentiles. The whiskers on the boxplot illustrate the 10th and 90th percentiles. Legend: * = p<0.05 (TIFF 7569 kb)

221_2019_5536_MOESM2_ESM.tif

Supplementary Fig.2: Results of the double-pulse stimulation test: A) Typical example of the averaged waveform of the responses elicited by double-pulse stimulation (n=1) in multiple lower-limb muscles. tSCS was delivered at 0 ms and 50 ms. B) Medians (n=8) of the peak to-peak amplitude of both the first and the second response. The lines in the box plots indicate the medians. The ends of the boxes represent the 25th and 75th percentiles. The whiskers on the boxplot illustrate the 10th and 90th percentiles. Legend: * = p<0.05 (TIFF 7047 kb)

221_2019_5536_MOESM3_ESM.tif

Supplementary Fig. 3: Background EMG activity as observed in experiment 1. Filled circles represent the mean (n=8). Unfilled circles represent the individual data points from each participant (TIFF 3890 kb)

221_2019_5536_MOESM4_ESM.tif

Supplementary Fig.4: Background EMG activity as observed in experiment 2. The lines in the box plots indicate median values. The ends of the boxes represent the 25th and 75th percentiles. The whiskers on the boxplot illustrate the 10th and 90th percentiles. Legend: * = p<0.05 (TIFF 2118 kb)

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Masugi, Y., Sasaki, A., Kaneko, N. et al. Remote muscle contraction enhances spinal reflexes in multiple lower-limb muscles elicited by transcutaneous spinal cord stimulation. Exp Brain Res 237, 1793–1803 (2019). https://doi.org/10.1007/s00221-019-05536-9

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