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Characterizing the effect of low intensity transcranial magnetic stimulation on the soleus H-reflex at rest

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Abstract

Modulation of a Hoffmann (H)-reflex following transcranial magnetic stimulation (TMS) has been used to assess the nature of signals transmitted from cortical centers to lower motor neurons. Further characterizing the recruitment and time-course of the TMS-induced effect onto the soleus H-reflex adds to the discussion of these pathways and may improve its utility in clinical studies. In 10 healthy controls, TMS was used to condition the soleus H-reflex using TMS intensities from 65 to 110% of the resting motor threshold (RMT). Early facilitation [− 5 to − 3 ms condition-test (C-T) interval] was evident when TMS was 110% of RMT (P < 0.05). By comparison, late facilitation (+ 10 to + 20 ms C-T interval) was several times larger and observed over a wider range of TMS intensities, including 65–110% of RMT. The early inhibition (− 3 to − 1 ms C-T interval) had a low TMS threshold and was elicited over a wide range of intensity from 65% to 95% of RMT (all P < 0.05). A second inhibitory phase was seen ~ 4 ms later (+ 1 to + 4 ms C-T intervals) and was only observed for a TMS intensity of 95% of RMT (P < 0.05). The present findings reaffirm that subthreshold TMS strongly modulates soleus motor neurons and demonstrates that distinct pathways can be selectively probed at discrete C-T intervals when using specific TMS intensities.

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References

  • Alvarez R, Valls-Solé J, Valldeoriola F (1995) Abnormal modulation of the soleus H reflex by transcranial cortical magnetic stimuli in patients with Parkinson’s disease. Electroencephalogr Clin Neurophysiol Electromyogr Motor Control 4:S194

    Google Scholar 

  • Andrews JC, Stein RB, Roy FD (2015a) Post-activation depression in the human soleus muscle using peripheral nerve and transcutaneous spinal stimulation. Neurosci Lett 589:144–149

    CAS  Google Scholar 

  • Andrews JC, Stein RB, Roy FD (2015b) Reduced postactivation depression of soleus H reflex and root evoked potential after transcranial magnetic stimulation. J Neurophysiol 114:485–492

    CAS  Google Scholar 

  • Andrews JC, Stein RB, Jones KE, Hedden DM, Mahood JK, Moreau MJ, Huang EM, Roy FD (2016) Intraoperative spinal cord monitoring using low intensity transcranial stimulation to remove post-activation depression of the H-reflex. Clin Neurophysiol 127:3378–3384

    Google Scholar 

  • Andrews JC, Roy FD, Stein RB, Ba F, Sankar T (2020) Effects of deep brain stimulation and dopaminergic medication on excitatory and inhibitory spinal pathways in Parkinson’s disease. J Clin Neurophysiol (Online ahead of print)

  • Bawa P, Chalmers GR, Stewart H, Eisen AA (2002) Responses of ankle extensor and flexor motoneurons to transcranial magnetic stimulation. J Neurophysiol 88:124–132

    CAS  Google Scholar 

  • Brouwer B, Ashby P (1992) Corticospinal projections to lower limb motoneurons in man. Exp Brain Res 89:649–654

    CAS  Google Scholar 

  • Costa J, Guzmán J, Valldeoriola F, Rumià J, Tolosa E, Casanova-Molla J, Valls-Solé J (2011) Modulation of the soleus H reflex by electrical subcortical stimuli in humans. Exp Brain Res 212:439–448

    Google Scholar 

  • Cowan JM, Day BL, Marsden C, Rothwell JC (1986) The effect of percutaneous motor cortex stimulation on H reflexes in muscles of the arm and leg in intact man. J Physiol (Lond) 377:333–347

    CAS  Google Scholar 

  • Delwaide PJ, Pepin JL, Maertens de Noordhout A (1991) Short-latency autogenic inhibition in patients with Parkinsonian rigidity. Ann Neurol 30:83–89

    CAS  Google Scholar 

  • Delwaide PJ, Pepin JL, De Pasqua V, de Noordhout AM (2000) Projections from basal ganglia to tegmentum: a subcortical route for explaining the pathophysiology of Parkinson’s disease signs? J Neurol 247(Suppl 2):II7–II1181

    Google Scholar 

  • Di Lazzaro V, Ziemann U, Lemon RN (2008) State of the art: Physiology of transcranial motor cortex stimulation. Brain Stimul 1:345–362

    Google Scholar 

  • Eccles JC (1964) The physiology of synapses. Springer, Berlin, p 316

    Book  Google Scholar 

  • Hultborn H, Illert M, Nielsen J, Paul A, Ballegaard M, Wiese H (1996) On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp Brain Res 108:450–462

    Article  CAS  Google Scholar 

  • Iles JF (1996) Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb. J Physiol 491:197–207

    Article  CAS  Google Scholar 

  • Iles JF, Pisini JV (1992) Cortical modulation of transmission in spinal reflex pathways of man. J Physiol 455:425–446

    Article  CAS  Google Scholar 

  • Jankowska E, Lund S, Lundberg A, Pompeiano O (1968) Inhibitory effects evoked through ventral reticulospinal pathways. Arch Ital Biol 106:124–140

    CAS  Google Scholar 

  • Kurz A, Xu W, Wiegel P, Leukel C, Baker SN (2019) Non-invasive assessment of superficial and deep layer circuits in human motor cortex. J Physiol 597(12):2975–2991

    Article  CAS  Google Scholar 

  • Kuypers HGJM (1981) Anatomy of the descending pathways. In: Handbook of physiology, sect. I the nervous system. American Physiology Society, Bethesda, MD, Wiley-Blackwell, pp 597–666

  • Lauber B, Gollhofer A, Taube W (2018) Differences in motor cortical control of the soleus and tibialis anterior. J Exp Biol 221:1–8

    Google Scholar 

  • Meunier S (1999) Modulation by corticospinal volleys of presynaptic inhibition to Ia afferents in man. J Physiol Paris 93:387–394

    CAS  Google Scholar 

  • Misiaszek JE (2003) The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 28:144–160

    Google Scholar 

  • Morita H, Olivier E, Baumgarten J, Petersen N, Christensen LO, Nielsen JB (2000) Differential changes in corticospinal and Ia input to tibialis anterior and soleus motor neurones during voluntary contraction in man. Acta Physiol Scand 170:65–76

    CAS  Google Scholar 

  • Morita H, Shindo M, Morita S, Hashimoto T, Tada T, Ikeda S (2002) Abnormal conditioning effect of transcranial magnetic stimulation on soleus H-reflex during voluntary movement in Parkinson’s disease. Clin Neurophysiol 113:1316–1324

    CAS  Google Scholar 

  • Nielsen J, Petersen N (1995a) Changes in the effect of magnetic brain stimulation accompanying voluntary dynamic contraction in man. J Physiol (Lond) 484(Pt 3):777–789

    CAS  Google Scholar 

  • Nielsen J, Petersen N (1995b) Evidence favouring different descending pathways to soleus motoneurones activated by magnetic brain stimulation in man. J Physiol (Lond) 486(Pt 3):779–788

    CAS  Google Scholar 

  • Nielsen J, Petersen N, Deuschl G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol (Lond) 471:223–243

    CAS  Google Scholar 

  • Niemann N, Wiegel P, Kurz A, Rothwell JC, Leukel C (2018) Assessing TMS-induced D and I waves with spinal H-reflexes. J Neurophysiol 119:933–943

    Google Scholar 

  • Palmieri RM, Ingersoll CD, Hoffman MA (2004) The Hoffmann Reflex: methodologic considerations and applications for use in sports medicine and athletic training research. J Athl Train 39(3):268–277

    Google Scholar 

  • Phillips CG, Porter R (1977) Corticospinal neurones. Their role in movement. Monogr Physiol Soc 34:1–450

    Google Scholar 

  • Pierrot-Deseilligny E, Mazevet D (2000) The monosynaptic reflex: a tool to investigate motor control in humans. Interests and limits. Clin Neurophysiol 30(2):67–80

    CAS  Google Scholar 

  • Pierrot-Desseilligny E, Burke D (2005) The circuitry of the human spinal cord: Its role in motor control and movement disorders. Cambridge University Press. Cambridge, UK, pp 7–188

    Google Scholar 

  • Pötter-Nerger M, Ilic TV, Siebner HR, Deuschl G, Volkmann J (2008) Subthalamic nucleus stimulation restores corticospinal facilitation in Parkinson’s disease. Mov Disord 23:2210–2215

    Google Scholar 

  • Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200

    CAS  Google Scholar 

  • Rudomin P (1990) Presynaptic inhibition of muscle spindle and tendon organ afferents in mammalian spinal cord. Trends Neurosci 13:499–505

    CAS  Google Scholar 

  • Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I (1997) Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil. Exp Brain Res 113:24–32

    Article  CAS  Google Scholar 

  • Serranová T, Valls-Solé J, Muñoz E, Genís D, Jech R, Seeman P (2008) Abnormal corticospinal tract modulation of the soleus H reflex in patients with pure spastic paraparesis. Neurosci Lett 437:15–19

    Article  Google Scholar 

  • Swadlow HA (1994) Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J Neurophysiol 71:437–453

    Article  CAS  Google Scholar 

  • Takakusaki K, Ohta Y, Mori S (1989) Single medullary reticulospinal neurons exert postsynaptic inhibitory effects via inhibitory interneurons upon alpha-motoneurons innervating cat hindlimb muscles. Exp Brain Res 74:11–23

    Article  CAS  Google Scholar 

  • Valls-Solé J, Alvarez R, Tolosa ES (1994) Vibration-induced presynaptic inhibition of the soleus H reflex is temporarily reduced by cortical magnetic stimulation in human subjects. Neurosci Lett 170:149–152

    Google Scholar 

  • Wiegel P, Kurz A, Leukel C (2020) Evidence that distinct human primary motor cortex circutis control discrete and rhythmic movements. J Physiol 598(6):1235–1251

    CAS  Google Scholar 

Download references

Acknowledgements

Jennifer Andrews Ph.D. was supported by a Parkinson Association of Alberta post-doctoral fellowship award. This work was supported in part by the University of Alberta Hospital Foundation (Kaye Fund, Dr. Tejas Sankar Research Establishment Grant and the Karen Bain and David Baine Movement Disorder Research Fund), and the Charles H. Backman Fund.

Funding

Parkinson Association of Alberta, University of Alberta Hospital Foundation (Kaye Fund, Dr. Tejas Sankar Research Establishment Grant and the Karen Bain and David Baine Movement Disorder Research Fund), and the Charles H. Backman Fund.

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Authors and Affiliations

  1. Department of Surgery, University of Alberta Hospital, WMC 1C3.13, Edmonton, AB, T6G 2E1, Canada

    Jennifer C. Andrews & François D. Roy

  2. Division of Neurosurgery, University of Alberta, Edmonton, Canada

    Tejas Sankar

  3. Department of Physiology, University of Alberta, Edmonton, Canada

    Richard B. Stein

Authors
  1. Jennifer C. Andrews
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  2. Tejas Sankar
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  3. Richard B. Stein
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  4. François D. Roy
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Correspondence to François D. Roy.

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Research approved by the Health Ethics Board at the University of Alberta.

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All participants provided written informed consent to the experimental protocol approved by the Health Ethics Board at the University of Alberta.

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Communicated by Winston D. Byblow.

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Andrews, J.C., Sankar, T., Stein, R.B. et al. Characterizing the effect of low intensity transcranial magnetic stimulation on the soleus H-reflex at rest. Exp Brain Res 238, 2725–2731 (2020). https://doi.org/10.1007/s00221-020-05879-8

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  • DOI: https://doi.org/10.1007/s00221-020-05879-8

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