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Review

Paired associative stimulation to enhance motor outcome in spinal cord injury: a systematic review of first evidence

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Pages 507-518 | Received 21 Feb 2024, Accepted 17 May 2024, Published online: 30 May 2024

References

  • Bennett J, Das M, Emmady PD. Spinal cord injuries 2022 May 11. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023 Jan. PMID: 32809556.
  • van Den Hauwe L, Sundgren PC, Flanders AE. Spinal Trauma and spinal cord injury (SCI). 2020 Feb 15. In: Hodler J, Kubik-Huch R von Schulthess G, editors. Diseases of the brain, head and neck, spine 2020–2023: diagnostic Imaging [Internet]. Cham (CH): Springer; 2020. Chapter 19. PMID: 32119240.
  • Fehlings MG, Vaccaro AR, Boakye M, et al. Burns essentials of spinal cord injury basic research to clinical practice. Denver (CO) (USA): Thieme Medical Publishers Inc.; 2013.
  • Silva NA, Sousa N, Reis RL, et al. From basics to clinical: a comprehensive review on spinal cord injury. Prog Neurobiol. 2014 Mar;114:25–57. doi: 10.1016/j.pneurobio.2013.11.002 Epub 2013 Nov 20. PMID: 24269804.
  • Cajigas I, Vedantam A. Brain-computer interface, neuromodulation, and neurorehabilitation strategies for spinal cord injury. Neurosurg Clin N Am. 2021 Jul;32(3):407–417. doi: 10.1016/j.nec.2021.03.012 Epub 2021 May 7. PMID: 34053728.
  • Kaneko N, Sasaki A, Masugi Y, et al. The effects of paired associative stimulation with transcutaneous spinal cord stimulation on corticospinal excitability in multiple lower-limb muscles. Neuroscience. 2021 Nov 10;476:45–59. doi: 10.1016/j.neuroscience.2021.08.028 Epub 2021 Sep 7. PMID: 34500017.
  • Shulga A, Lioumis P, Kirveskari E, et al. The use of F-response in defining interstimulus intervals appropriate for LTP-like plasticity induction in lower limb spinal paired associative stimulation. J Neurosci Methods. 2015 Mar 15;242:112–117. doi: 10.1016/j.jneumeth.2015.01.012 Epub 2015 Jan 15. PMID: 25597909.
  • Hashemirad F, Zoghi M, Fitzgerald PB, et al. Reliability of motor evoked potentials induced by transcranial magnetic stimulation: the effects of initial motor evoked potentials removal. Basic Clin Neurosci. 2017 Jan;8(1):43–50. doi: 10.15412/J.BCN.03080106 PMID: 28446949; PMCID: PMC5396172.
  • Fisher MA. F-waves–physiology and clinical uses. Sci World J. 2007 Feb 2;7:144–160. doi: 10.1100/tsw.2007.49
  • Carson RG, Kennedy NC. Modulation of human corticospinal excitability by paired associative stimulation. Front Hum Neurosci. 2013 Dec 3;7:823. doi: 10.3389/fnhum.2013.00823 PMID: 24348369; PMCID: PMC3847812.
  • Koch G, Ponzo V, Di Lorenzo F, et al. Hebbian and anti-Hebbian spike-timing-dependent plasticity of human cortico-cortical connections. J Neurosci. 2013 Jun 5;33(23):9725–9733. doi: 10.1523/JNEUROSCI.4988-12.2013 PMID: 23739969; PMCID: PMC6619701.
  • Ceccanti M, Onesti E, Rubino A, et al. Modulation of human corticospinal excitability by paired associative stimulation in patients with amyotrophic lateral sclerosis and effects of Riluzole. Brain Stimul. 2018 Jul;11(4):775–781. doi: 10.1016/j.brs.2018.02.007 Epub 2018 Feb 7. PMID: 29459142.
  • Alokaily AO, Yarossi M, Fluet GG, et al. The effect of movement phase on the contralaterally coordinated paired associative stimulation-induced excitability. Annu Int Conf IEEE Eng Med Biol Soc. 2018 Jul;2018:3080–3083. doi: 10.1109/EMBC.2018.8512931 PMID: 30441045; PMCID: PMC6457650.
  • Fok KL, Kaneko N, Sasaki A, et al. Motor point stimulation in spinal paired associative stimulation can facilitate spinal cord excitability. Front Hum Neurosci. 2020 Nov 27;14:593806. doi: 10.3389/fnhum.2020.593806 PMID: 33328940; PMCID: PMC7729006.
  • Stefan K, Kunesch E, Cohen LG, et al. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 2000 Mar;123(3):572–584. doi: 10.1093/brain/123.3.572 PMID: 10686179.
  • Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009 Jul 21;339(jul21 1):b2535. doi: 10.1136/bmj.b2535
  • Eriksen MB, Frandsen TF. The impact of patient, intervention, comparison, outcome (PICO) as a search strategy tool on literature search quality: a systematic review. J Med Libr Assoc. 2018 Oct;106(4):420–431. doi: 10.5195/jmla.2018.345 Epub 2018 Oct 1. PMID: 30271283; PMCID: PMC6148624.
  • Ouzzani M, Hammady H, Fedorowicz Z, et al. Rayyan-a web and mobile app for systematic reviews. Syst Rev. 2016 Dec 5;5(1):210. doi: 10.1186/s13643-016-0384-4 PMID: 27919275; PMCID: PMC5139140.
  • Sterne JAC, Savović J, Page MJ, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ. 2019;366:l4898. doi: 10.1136/bmj.l4898
  • Quality Assessment Tool for Case Series studies. National heart, lung, and blood institute. Available from: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools.
  • Zhang Z, Lin BS, Peng CW, et al. Design of a novel paired associative nerve stimulation system and treatment strategy for incomplete spinal cord injury: a preliminary study. IEEE Trans Neural Syst Rehabil Eng. 2021;29:1341–1349. doi: 10.1109/TNSRE.2021.3095842
  • Versace V, Langthaler PB, Höller Y, et al. Abnormal cortical neuroplasticity induced by paired associative stimulation after traumatic spinal cord injury: a preliminary study. Neurosci Lett. 2018 Jan 18;664:167–171. doi: 10.1016/j.neulet.2017.11.003
  • Shulga A, Zubareva A, Lioumis P, et al. Paired associative stimulation with high-frequency peripheral component leads to enhancement of corticospinal transmission at wide range of interstimulus intervals. Front Hum Neurosci. 2016 Sep 23;10:470. doi: 10.3389/fnhum.2016.00470
  • Pohjonen M, Savolainen S, Arokoski J, et al. Omitting TMS component from paired associative stimulation with high-frequency PNS: a case series of tetraplegic patients. Clin Neurophysiol Pract. 2021 Feb 20;6:81–87. doi: 10.1016/j.cnp.2021.01.004 PMID: 33748549; PMCID: PMC7970010.
  • Grover FM, Chen B, Perez MA. Increased paired stimuli enhance corticospinal-motoneuronal plasticity in humans with spinal cord injury. J Neurophysiol. 2023 Jun 1;129(6):1414–1422. doi: 10.1152/jn.00499.2022
  • Mao YR, Jin ZX, Zheng Y, et al. Effects of cortical intermittent theta burst stimulation combined with precise root stimulation on motor function after spinal cord injury: a case series study. Neural Regen Res. 2022 Aug;17(8):1821–1826. doi: 10.4103/1673-5374.332158
  • Sun TT, Zhu GY, Zheng Y, et al. Effects of paired associative magnetic stimulation between nerve root and cortex on motor function of lower limbs after spinal cord injury: study protocol for a randomized controlled trial. Neural Regen Res. 2022 Nov;17(11):2459–2464. doi: 10.4103/1673-5374.339012. PMID: 35535897; PMCID: PMC9120678.
  • Perez M. Effects of paired associative magnetic stimulation between nerve root and cortex on motor function of lower limbs after spinal cord injury: study protocol for a randomized controlled trial. Brain Stimul. 2023 Jan;16(1):168.
  • Jo HJ, Perez MA. Corticospinal-motor neuronal plasticity promotes exercise-mediated recovery in humans with spinal cord injury. Brain. 2020 May 1;143(5):1368–1382. doi: 10.1093/brain/awaa052 PMID: 32355959; PMCID: PMC7534104.
  • Rodionov A, Savolainen S, Kirveskari E, et al. Restoration of hand function with long-term paired associative stimulation after chronic incomplete tetraplegia: a case study. Spinal Cord Ser Cases. 2019 Oct 1;5:81. doi: 10.1038/s41394-019-0225-5 PMID: 31632739; PMCID: PMC6786383.
  • Rodionov A, Savolainen S, Kirveskari E, et al. Effects of long-term paired associative stimulation on strength of leg muscles and walking in chronic tetraplegia: a proof-of-concept pilot study. Front Neurol. 2020 May 20;11:397. doi: 10.3389/fneur.2020.00397 PMID: 32508738; PMCID: PMC7251052.
  • Shulga A, Lioumis P, Zubareva A, et al. Long-term paired associative stimulation can restore voluntary control over paralyzed muscles in incomplete chronic spinal cord injury patients. Spinal Cord Ser Cases. 2016 Jul 14;2:16016. doi: 10.1038/scsandc.2016.16 PMID: 28053760; PMCID: PMC5129397.
  • Shulga A, Savolainen S, Kirveskari E, et al. Enabling and promoting walking rehabilitation by paired associative stimulation after incomplete paraplegia: a case report. Spinal Cord Ser Cases. 2020 Aug 13;6(1):72. doi: 10.1038/s41394-020-0320-7 PMID: 32792474; PMCID: PMC7426433.
  • Tolmacheva A, Savolainen S, Kirveskari E, et al. Long-term paired associative stimulation enhances motor output of the tetraplegic hand. J Neurotrauma. 2017 Sep 15;34(18):2668–2674. doi: 10.1089/neu.2017.4996 Epub 2017 Jul 21. PMID: 28635523; PMCID: PMC5610384.
  • Tolmacheva A, Savolainen S, Kirveskari E, et al. Paired associative stimulation improves hand function after non-traumatic spinal cord injury: a case series. Clin Neurophysiol Pract. 2019 Aug 13;4:178–183. doi: 10.1016/j.cnp.2019.07.002 PMID: 31886442; PMCID: PMC6921158.
  • Vaalto S, Nyman AL, Shulga A. Analgesic effect of paired associative stimulation in a tetraplegic patient with severe drug-resistant neuropathic pain: a case report. Scand J Pain. 2021 May 21;21(4):831–838. doi: 10.1515/sjpain-2021-0012 PMID: 34019752.
  • Pulverenti TS, Zaaya M, Grabowski M, et al. Neurophysiological changes after paired brain and spinal cord stimulation coupled with locomotor training in human spinal cord injury. Front Neurol. 2021 May 10;12:627975. doi: 10.3389/fneur.2021.627975 PMID: 34040572; PMCID: PMC8141587.
  • Pulverenti TS, Zaaya M, Knikou M. Brain and spinal cord paired stimulation coupled with locomotor training affects polysynaptic flexion reflex circuits in human spinal cord injury. Exp Brain Res. 2022 Jun;240(6):1687–1699. doi: 10.1007/s00221-022-06375-x Epub 2022 May 6. PMID: 35513720; PMCID: PMC9215206.
  • Mezes M, Havu R, Tolmacheva A, et al. The impact of TMS and PNS frequencies on MEP potentiation in PAS with high-frequency peripheral component. PLOS ONE. 2020 May 29;15(5):e0233999. doi: 10.1371/journal.pone.0233999 PMID: 32470028; PMCID: PMC7259644.
  • Sathya GR, Krishnamurthy N, Veliath S, et al. F wave index: a diagnostic tool for peripheral neuropathy. Indian J Med Res. 2017 Mar;145(3):353–357. doi: 10.4103/ijmr.IJMR_1087_14 PMID: 28749398; PMCID: PMC5555064.
  • Vallence AM, Rurak BK, Fujiyama H, et al. Covariation of the amplitude and latency of motor evoked potentials elicited by transcranial magnetic stimulation in a resting hand muscle. Exp Brain Res. 2023 Mar;241(3):927–936. doi: 10.1007/s00221-023-06575-z Epub 2023 Feb 22. PMID: 36811686; PMCID: PMC9985579.
  • Guidali G, Roncoroni C, Bolognini N. Paired associative stimulations: novel tools for interacting with sensory and motor cortical plasticity. Behav Brain Res. 2021;414:113484. doi: 10.1016/j.bbr.2021.113484
  • Alder G, Signal N, Olsen S, et al. A systematic review of paired associative stimulation (PAS) to modulate lower limb corticomotor excitability: implications for stimulation parameter selection and experimental design. Front Neurosci. 2019 Aug 27;13:895. doi: 10.3389/fnins.2019.00895 PMID: 31507367; PMCID: PMC6718871.
  • Classen J, Wolters A, Stefan K, et al. Paired associative stimulation. Suppl Clin Neurophysiol. 2004;57:563–569.
  • Uy J, Ridding MC, Hillier S, et al. Does induction of plastic change in motor cortex improve leg function after stroke? Neurology. 2003 Oct 14;61(7):982–984. doi: 10.1212/01.wnl.0000078809.33581.1f PMID: 14557574.
  • Popp WL, Schneider S, Bär J, et al. wearable sensors in ambulatory individuals with aspinal cord injury: from energy expenditure estimation to activity recommendations. Front Neurol. 2019 Nov 1;10:1092. doi: 10.3389/fneur.2019.01092 PMID: 31736845; PMCID: PMC6838774.
  • Caballol N, Bayés À, Prats A, et al. Feasibility of a wearable inertial sensor to assess motor complications and treatment in Parkinson’s disease. PLOS ONE. 2023 Feb 2;18(2):e0279910. doi: 10.1371/journal.pone.0279910 PMID: 36730238; PMCID: PMC9894418.
  • Martino Cinnera A, Picerno P, Bisirri A, et al. Upper limb assessment with inertial measurement units according to the international classification of functioning in stroke: a systematic review and correlation meta-analysis. Top Stroke Rehabil. 2023 Apr;31(1):66–85. doi: 10.1080/10749357.2023.2197278 Epub ahead of print. PMID: 37083139.
  • Lefaucheur JP, Aleman A, Baeken C, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): An update (2014-2018). Clin Neurophysiol. 2020 Feb;131(2):474–528. doi: 10.1016/j.clinph.2019.11.002 Epub 2020 Jan 1. Erratum in: Clin Neurophysiol. 2020 May;131(5):1168-1169. PMID: 31901449.
  • de Araújo AVL, Neiva JFO, Monteiro CBM, et al. Efficacy of virtual reality rehabilitation after spinal cord injury: a systematic review. Biomed Res Int. 2019 Nov 13;2019:1–15. doi: 10.1155/2019/7106951 PMID: 31828120; PMCID: PMC6885151.
  • Morone G, de Sire A, Martino Cinnera A, et al. Upper limb robotic rehabilitation for patients with cervical spinal cord injury: a comprehensive review. Brain Sci. 2021 Dec 10;11(12):1630. doi: 10.3390/brainsci11121630 PMID: 34942935; PMCID: PMC8699455.
  • Sathyan S, Tolmacheva A, Tugin S, et al. A new paired associative stimulation protocol with high-frequency peripheral component and high-intensity 20 Hz repetitive transcranial magnetic stimulation-a pilot study. Int j environ res public health. 2021 Oct 26;18(21):11224. doi: 10.3390/ijerph182111224 PMID: 34769744; PMCID: PMC8583447.

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