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Cortical and Subcortical Effects of Transcutaneous Spinal Cord Stimulation in Humans with Tetraplegia

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Cortical and Subcortical Effects of Transcutaneous Spinal Cord Stimulation in Humans with Tetraplegia Research Articles: Development/Plasticity/Repair Cortical and Subcortical Effects of Transcutaneous Spinal Cord Stimulation in Humans with Tetraplegia https://doi.org/10.1523/JNEUROSCI.2374-19.2020 Cite as: J. Neurosci 2020; 10.1523/JNEUROSCI.2374-19.2020 Received: 3 October 2019 Revised: 9 January 2020 Accepted: 17 January 2020 This Early Release article has been peer-reviewed and accepted, but has not been through the composition and copyediting processes. The final version may differ slightly in style or formatting and will contain links to any extended data. Alerts: Sign up at www.jneurosci.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Copyright © 2020 the authors 1 Cortical and Subcortical Effects of Transcutaneous Spinal Cord Stimulation in 2 Humans with Tetraplegia 3 4 5 6 Francisco D. Benavides1,2,3, Hang Jin Jo1,2,3, Henrik Lundell4, V. Reggie Edgerton5,6,7,8,9,10, Yuri 7 Gerasimenko5,6,11, and Monica A. Perez1,2,3 8 1Department of Neurological Surgery, The Miami Project to Cure Paralysis, University of 9 Miami, Florida, US; 2Shirley Ryan Ability Lab and Northwestern University, Chicago, US 10 3Hines VA Medical Center, Chicago, US; 4Danish Research Centre for Magnetic Resonance, 11 Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital 12 Hvidovre, Hvidovre, Denmark; 5Department of Integrative Biology and Physiology, California, 13 US; 6Neurobiology, and 7Neurosurgery, University of California Los Angeles; 8Brain Research 14 Institute; 9Institut Guttmann, Hospital de Neurorehabilitació, Universitat Autònoma de 15 Barcelona, Badalona, Spain California, US; 10Centre for Neuroscience and Regenerative 16 Medicine, Faculty of Science, University of Technology Sydney, Australia; 11Pavlov Institute of 17 Physiology, St.Petersburg, Russia 18 19 20 21 22 Corresponding author: 23 Monica A. Perez, PT, PhD 24 Scientific Chair Arms + Hands AbilityLab 25 Professor PM&R 26 Research Scientist Hines VA 27 312-238-2886 office 28 312-238-6636 fax 29 [email protected] 30 31 Section and Senior Editor: 32 Abbreviated title: Spinal cord stimulation after tetraplegia 33 Number of figures: 7 34 Number of tables: 1 35 Number of pages: 38 36 37 Key words: Neuroplasticity, spinal cord injury, spinal networks, intracortical inhibition, 38 neurophysiology, corticospinal 39 40 1 41 Abstract 42 An increasing number of studies support the view that transcutaneous electrical 43 stimulation of the spinal cord (TESS) promotes functional recovery in humans with spinal cord 44 injury (SCI). However, the neural mechanisms contributing to these effects remain poorly 45 understood. Here we examined motor evoked potentials in arm muscles elicited by cortical and 46 subcortical stimulation of corticospinal axons before and after 20 min of TESS (30Hz pulses 47 with a 5kHz carrier frequency) and sham-TESS applied between C5–C6 spinous processes in 48 males and females with and without chronic incomplete cervical SCI. The amplitude of 49 subcortical but not cortical motor evoked responses increased in proximal and distal arm muscles 50 for 75 min after TESS, but not sham-TESS, in controls and SCI participants, suggesting a 51 subcortical origin for these effects. Intracortical inhibition, elicited by paired stimuli, increased 52 after TESS in both groups. When TESS was applied without the 5kHz carrier frequency both 53 subcortical and cortical motor evoked responses were facilitated without changing intracortical 54 inhibition, suggesting that the 5kHz carrier frequency contributed to the cortical inhibitory 55 effects. Hand and arm function improved largely when TESS was used with, compared to 56 without the 5kHz carrier frequency. These novel observations demonstrate that TESS influence 57 cortical and spinal networks, having an excitatory effect at the spinal level and an inhibitory 58 effect at the cortical level. We hypothesized that these parallel effects contribute to further the 59 recovery of limb function following SCI. 60 61 62 63 2 64 Significance statement 65 Accumulating evidence supports the view that transcutaneous electrical stimulation of the 66 spinal cord (TESS) promotes recovery of function in humans with spinal cord injury (SCI). Here, 67 we show that a single session of TESS over the cervical spinal cord in individuals with 68 incomplete chronic cervical SCI influenced in parallel the excitability cortical and spinal 69 networks, having an excitatory effect at the spinal level and an inhibitory effect at the cortical 70 level. Importantly, these parallel physiological effects had an impact of the magnitude of 71 improvements in voluntary motor output. 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 3 87 Introduction 88 An increasing number of studies support the view that transcutaneous electrical 89 stimulation of the spinal cord (TESS) promotes functional recovery in humans with spinal cord 90 injury (SCI). TESS has shown improvements in sensory and motor function when it is applied 91 alone or in combination with other therapies (Hofstoetter et al., 2013; Gerasimenko et al, 2015; 92 Inanici et al., 2018; Gad et al., 2017, 2018). Improved cardiovascular (Phillips et al., 2018) and 93 bladder (Horst et al., 2013; Radziszewski et al., 2013) functions and reduced spasticity 94 (Hofstoetter et al., 2014, 2019) have also been observed. While it is clear that single TESS pulses 95 generate spinally-mediated responses activating spinal networks that project transsynaptically to 96 motoneurons (Milosevic et al., 2019) the effects of repeated use of TESS on central nervous 97 system (CNS) pathways remain unknown. A more complete understanding of the neural 98 mechanisms of TESS-induced recovery is likely to enhance rehabilitation effectiveness. 99 Electrophysiological (Minassian et al., 2007; Hofstoetter et al., 2018) and modelling 100 (Rattay et al., 2000; Capofrosso et al., 2013) studies suggest that a single TESS pulse recruits 101 large-to-medium diameter proprioceptive and cutaneous afferents within posterior rootlets/roots 102 of different spinal segments depending on the stimulus intensity. Most studies in humans with 103 SCI aiming to achieve therapeutic effects use TESS currents between 5–50Hz with intensities 104 fluctuating between 10–200 mA using a high carrier frequency between 5–10kHz for several 105 minutes to hours (see references above). In humans, a prolonged period of repeated stimulation 106 of afferent fibers in a peripheral nerve with frequencies between 5–50Hz usually increases the 107 net excitability of descending cortical-motor neuron pathways, perhaps by reducing the activity 108 of GABAergic cortical mechanisms (Kaelin-Lang et al., 2002; Golaszewski et al., 2012). Note 109 that TESS uses a high carrier frequency or a ‘Russian current’. Russian currents are alternating 4 110 currents in a frequency range from around 100Hz to 10kHz which are delivered in bursts, with a 111 burst frequency within a “physiological” range (up to ~100Hz; Ward et al., 2009). It is thought 112 that this high carrier frequency is beneficial for improving muscle strength (Selkowitz, 1985, 113 1989) and for suppressing the sensitivity of pain receptors (Eard et al., 1998a,b). High frequency 114 electrical stimulation of the spinal cord releases serotonin in the dorsal horn (Linderoth et al., 115 1993), which may depress ascending nociceptive transmission (Furst, 1999; Millan, 2002). 116 Indeed, stimulation of muscle afferents at frequencies around 100Hz have an inhibitory effect of 117 motor cortex (Mima et al., 2004). We hypothesized that TESS has a predominant excitatory 118 effect on spinal networks and predominantly inhibitory effects at the cortical level, both of which 119 could serve to fine-tune the net output that could contribute to further improving functional 120 recovery. 121 To test our hypothesis we evoked motor potentials in arm muscles by cortical and 122 subcortical stimulation of corticospinal axons before and after 20 min of TESS (30Hz pulses 123 with a 5kHz carrier frequency) applied between C5–C6 spinous processes in humans with and 124 without chronic incomplete cervical SCI. Structural magnetic resonance imaging (MRI) was 125 used to localize the extent of the spinal cord lesion and ensure that TESS was applied over 126 injured segments. 127 128 129 130 131 132 5 133 Materials and Methods 134 Participants. Seventeen individuals with SCI (mean age 43.1±14.0 years, 4 female) and 15 age- 135 matched controls (mean age 36.5±17.5 years, 6 female; p=0.3) participated in the study (Table 136 1). All participants gave informed consent to experimental procedures, which was approved by 137 the local ethics committee at the University of Miami in accordance with guidelines established 138 in the Declaration of Helsinki. Participants with SCI had a chronic injury (≥1 year) and were 139 classified using the International Standards for Neurological Classification of Spinal Cord Injury 140 (ISNCSCI) exam as having a C4–C6 SCI and by the American Spinal Cord Injury Association 141 Impairment Scale (AIS) as AIS A (n=4), AIS B (n=3), AIS C (n=2) or AIS D (n=8). Five SCI 142 individuals were taking anti-spastic medication (baclofen and/or gabapentin and/or tizanidine; 143 Table 1). 144 145 Study design. All subjects participated in the main experiment, in which a two-day cross-over 146 design was used to compare the effect of 20 min of TESS or sham-TESS, applied between C5– 147 C6 spinous processes, on motor evoked potentials elicited by transcranial magnetic stimulation 148 (MEPs) and by cervicomedullary electrical stimulation (CMEPs) in the biceps brachii. 149 Participants, but not experimenters, were blinded to the interventions. The duration of 150 stimulation was comparable to that used in other plasticity protocols targeting the spinal cord in 151 humans (Taylor and Martin, 2009; Bunday and Perez, 2012). The following tests were also 152 completed in additional sessions in a subset of subjects: (1) we examined the effect of 20 min of 153 TESS on MEPs and CMEPs elicited in the triceps brachii (controls=10; SCI=11) and first dorsal 154 interosseous (controls=8; SCI=8) muscles.
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