The effect of experimental pain on the excitability of the corticospinal tract in humans: A systematic review and meta-analysis.
Journal
European journal of pain (London, England)
ISSN: 1532-2149
Titre abrégé: Eur J Pain
Pays: England
ID NLM: 9801774
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
19
01
2021
received:
23
07
2020
accepted:
01
02
2021
pubmed:
11
2
2021
medline:
29
6
2021
entrez:
10
2
2021
Statut:
ppublish
Résumé
Pain influences motor control. Previous reviews observed that pain reduces the excitability of corticospinal projections to muscles tested with transcranial magnetic stimulation. However, the independent effect of the type of pain models (tonic, phasic), pain location and tissues targeted (e.g. muscle, skin) remains unexplored. The objective of this review was to determine the influence of experimental pain and of different methodological factors on the corticospinal excitability. Three electronic databases were searched: Embase, Pubmed and Web of Science. Meta-analyses were conducted in three consecutive steps to reduce methodological variability: (a) all studies; (b) same pain location; (c) same tissues, pain location and muscle state. Strength of evidence was assessed for each analysis performed. Forty studies were included in the review and 26 in the meta-analysis as it focused only on studies using tonic pain. Overall, there was conflicting/moderate evidence of a diminution of corticospinal excitability during and after tonic pain. When considering only pain location, tonic hand and face pain induced a reduction in corticospinal excitability (limited evidence). Both muscle and cutaneous hand pain reduced corticospinal excitability (limited/conflicting evidence). Similar results were observed for phasic pain (limited evidence). Our results confirm the inhibitory effect of pain on corticospinal excitability for both tonic and phasic pain. This reduction was specific to hand and face pain. Also, both cutaneous and muscle hand pain reduced excitability. The strength of evidence remains limited/conflicting. More high-quality studies are needed to confirm our conclusions. This study adds evidence on the effect of specific factors on the modulation of corticospinal excitability during/after experimental pain. The reduction in corticospinal excitability was driven by hand and face pain. We confirmed previous results that muscle pain reduces corticospinal excitability and provided evidence of a similar effect for cutaneous pain. Both models may inform on the influence of different types of pain on motor control. Future studies are needed to determine the origin of the effect of pain.
Sections du résumé
BACKGROUND AND OBJECTIVE
Pain influences motor control. Previous reviews observed that pain reduces the excitability of corticospinal projections to muscles tested with transcranial magnetic stimulation. However, the independent effect of the type of pain models (tonic, phasic), pain location and tissues targeted (e.g. muscle, skin) remains unexplored. The objective of this review was to determine the influence of experimental pain and of different methodological factors on the corticospinal excitability.
DATABASES AND DATA TREATMENT
Three electronic databases were searched: Embase, Pubmed and Web of Science. Meta-analyses were conducted in three consecutive steps to reduce methodological variability: (a) all studies; (b) same pain location; (c) same tissues, pain location and muscle state. Strength of evidence was assessed for each analysis performed.
RESULTS
Forty studies were included in the review and 26 in the meta-analysis as it focused only on studies using tonic pain. Overall, there was conflicting/moderate evidence of a diminution of corticospinal excitability during and after tonic pain. When considering only pain location, tonic hand and face pain induced a reduction in corticospinal excitability (limited evidence). Both muscle and cutaneous hand pain reduced corticospinal excitability (limited/conflicting evidence). Similar results were observed for phasic pain (limited evidence).
CONCLUSIONS
Our results confirm the inhibitory effect of pain on corticospinal excitability for both tonic and phasic pain. This reduction was specific to hand and face pain. Also, both cutaneous and muscle hand pain reduced excitability. The strength of evidence remains limited/conflicting. More high-quality studies are needed to confirm our conclusions.
SIGNIFICANCE
This study adds evidence on the effect of specific factors on the modulation of corticospinal excitability during/after experimental pain. The reduction in corticospinal excitability was driven by hand and face pain. We confirmed previous results that muscle pain reduces corticospinal excitability and provided evidence of a similar effect for cutaneous pain. Both models may inform on the influence of different types of pain on motor control. Future studies are needed to determine the origin of the effect of pain.
Types de publication
Journal Article
Meta-Analysis
Research Support, Non-U.S. Gov't
Review
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1209-1226Subventions
Organisme : Fonds de recherche du Québec - Santé
ID : 281961
Organisme : Fonds de recherche du Québec - Santé
ID : 289953
Informations de copyright
© 2021 European Pain Federation - EFIC®.
Références
Algoet, M., Duque, J., Iannetti, G. D., & Mouraux, A. (2018). Temporal profile and limb-specificity of phasic pain-evoked changes in motor excitability. Neuroscience, 386, 240-255. https://doi.org/10.1016/j.neuroscience.2018.06.039
Alhassani, G., Liston, M. B., & Schabrun, S. M. (2019). Interhemispheric inhibition is reduced in response to acute muscle pain: A cross-sectional study using transcranial magnetic stimulation. The Journal of Pain, 20, 1091-1099. https://doi.org/10.1016/j.jpain.2019.03.007
Andersen, O. K., Sonnenborg, F. A., & Arendt-Nielsen, L. (1999). Modular organization of human leg withdrawal reflexes elicited by electrical stimulation of the foot sole. Muscle and Nerve, 22,1520-1530. https://doi.org/10.1002/(SICI)1097-4598(199911)22:11<1520:AID-MUS6>3.0.CO;2-V
Andersen, O. K., Sonnenborg, F. A., & Arendt-Nielsen, L. (2001). Reflex receptive fields for human withdrawal reflexes elicited by non-painful and painful electrical stimulation of the foot sole. Clinical Neurophysiology, 112, 641-649. https://doi.org/10.1016/S1388-2457(01)00485-0
Bank, P. J. M., Peper, C. E., Marinus, J., Beek, P. J., & Van Hilten, J. J. (2013). Motor consequences of experimentally induced limb pain: A systematic review. European Journal of Pain, 17, 145-157. https://doi.org/10.1002/j.1532-2149.2012.00186.x
Barton, C. J., Lack, S., Malliaras, P., & Morrissey, D. (2013). Gluteal muscle activity and patellofemoral pain syndrome: A systematic review. British Journal of Sports Medicine, 47, 207-214. https://doi.org/10.1136/bjsports-2012-090953
Baumgärtner, U., Greffrath, W., & Treede, R. D. (2012). Contact heat and cold, mechanical, electrical and chemical stimuli to elicit small fiber-evoked potentials: Merits and limitations for basic science and clinical use. Neurophysiologie Clinique, 42, 267-280. https://doi.org/10.1016/j.neucli.2012.06.002
Beall, J. E., Applebaum, A. E., Foreman, R. D., & Willis, W. D. (1977). Spinal cord potentials evoked by cutaneous afferents in the monkey. Journal of Neurophysiology, 40, 199-211. https://doi.org/10.1152/jn.1977.40.2.199
Billot, M., Neige, C., Gagne, M., Mercier, C., & Bouyer, L. J. (2018). Effect of cutaneous heat pain on corticospinal excitability of the tibialis anterior at rest and during submaximal contraction. Neural Plasticity, 2018, 8713218. https://doi.org/10.1155/2018/8713218
Brouwer, B., & Ashby, P. (1992). Corticospinal projections to lower limb motoneurons in man. Experimental Brain Research, 89, 649-654. https://doi.org/10.1007/BF00229889
Burns, E., Chipchase, L. S., & Schabrun, S. M. (2016a). Primary sensory and motor cortex function in response to acute muscle pain: A systematic review and meta-analysis. European Journal of Pain, 20, 1203-1213.
Burns, E., Chipchase, L. S., & Schabrun, S. M. (2016b). Reduced short- and long-latency afferent inhibition following acute muscle pain: A potential role in the recovery of motor output. Pain Medicine, 17, 1343-1352.
Chen, R., Tam, A., Bütefisch, C., Corwell, B., Ziemann, U., Rothwell, J. C., & Cohen, L. G. (1998). Intracortical inhibition and facilitation in different representations of the human motor cortex. Journal of Neurophysiology, 80, 2870-2881.
Cheong, J. Y., Yoon, T. S., & Lee, S. J. (2003). Evaluations of inhibitory effect on the motor cortex by cutaneous pain via application of capsaicin. Electromyography and Clinical Neurophysiology, 43, 203-210.
Chipchase, L., Schabrun, S., Cohen, L., Hodges, P., Ridding, M., Rothwell, J., Taylor, J., & Ziemann, U. (2012). A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: An international consensus study. Clinical Neurophysiology, 123, 1698-1704.
Corbett, D. B., Simon, C. B., Manini, T. M., George, S. Z., Riley, J. L., & Fillingim, R. B. (2019). Movement-evoked pain: Transforming the way we understand and measure pain. Pain, 160, 757-761.
Cruccu, G., Aminoff, M. J., Curio, G., Guerit, J. M., Kakigi, R., Mauguiere, F., Rossini, P. M., Treede, R. D., & Garcia-Larrea, L. (2008). Recommendations for the clinical use of somatosensory-evoked potentials. Clinical Neurophysiology, 119, 1705-1719.
Darling, W. G., & Butler, A. J. (2006). Variability of motor potentials evoked by transcranial magnetic stimulation depends on muscle activation. Experimental Brain Research, 174, 376-385.
de Oliveira, F. C. L., Bouyer, L. J., Ager, A. L., & Roy, J. S. (2017). Electromyographic analysis of rotator cuff muscles in patients with rotator cuff tendinopathy: A systematic review. Journal of Electromyography & Kinesiology, 35, 100-114.
Delahunty, E. T., Bisset, L. M., & Kavanagh, J. J. (2019). Intracortical motor networks are affected in both the contralateral and ipsilateral hemisphere during single limb cold water immersion. Experimental Physiology, 104, 1296-1305.
DelSanto, F., Gelli, F., Spidalieri, R., & Rossi, A. (2007). Corticospinal drive during painful voluntary contractions at constant force output. Brain Research, 1128, 91-98.
DiLazzaro, V., Restuccia, D., Oliviero, A., Profice, P., Ferrara, L., Insola, A., Mazzone, P., Tonali, P., & Rothwell, J. C. (1998). Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. The Journal of Physiology, 2, 625-633.
Fadiga, L., Craighero, L., Dri, G., Facchin, P., Destro, M. F., & Porro, C. A. (2004). Corticospinal excitability during painful self-stimulation in humans: A transcranial magnetic stimulation study. Neuroscience Letters, 361, 250-253. https://doi.org/10.1016/j.neulet.2003.12.016
Farina, S., Tinazzi, M., Le Pera, D., & Valeriani, M. (2003). Pain-related modulation of the human motor cortex. Neurological Research, 25, 130-142. https://doi.org/10.1179/016164103101201283
Farina, S., Valeriani, M., Rosso, T., Aglioti, S., Tamburin, S., Fiaschi, A., & Tinazzi, M. (2001). Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation. Neuroscience Letters, 314, 97-101. https://doi.org/10.1016/S0304-3940(01)02297-2
Ferbert, A., Caramia, D., Priori, A., Bertolasi, L., & Rothwell, J. C. (1992). Cortical projection to erector spinae muscles in man as assessed by focal transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol Evoked Potentials, 85, 382-387. https://doi.org/10.1016/0168-5597(92)90051-C
Gelnar, P. A., Krauss, B. R., Sheehe, P. R., Szeverenyi, N. M., & Apkarian, A. V. (1999). A comparative fMRI study of cortical representations for thermal painful, vibrotactile, and motor performance tasks. NeuroImage, 10, 460-482. https://doi.org/10.1006/nimg.1999.0482
Gibbons, R. D., Hedeker, D. R., & Davis, J. M. (1993). Estimation of ES from a series of experiments involving paired comparisons. Journal of Educational and Behavioral Statistics, 18, 271-279.
Granovsky, Y., Sprecher, E., & Sinai, A. (2019). Motor corticospinal excitability: A novel facet of pain modulation? Pain Reports, 4, e725.-https://doi.org/10.1097/PR9.0000000000000725
Halkjaer, L., Melsen, B., McMillan, A. S., & Svensson, P. (2006). Influence of sensory deprivation and perturbation of trigeminal afferent fibers on corticomotor control of human tongue musculature. Experimental Brain Research, 170, 199-205. https://doi.org/10.1007/s00221-005-0199-3
Henderson, L. A., Bandler, R., Gandevia, S. C., & Macefield, V. G. (2006). Distinct forebrain activity patterns during deep versus superficial pain. Pain, 120, 286-296. https://doi.org/10.1016/j.pain.2005.11.003
Higgins, J., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M., & Welch, V. (2019). Cochrane Handbook for Systematic Reviews of Interventions version 6.0 (updated July 2019).
Hodges, P. W., & Smeets, R. J. (2015). Interaction between pain, movement, and physical activity: Short-term benefits, long-term consequences, and targets for treatment. Clinical Journal of Pain, 31, 97-107. https://doi.org/10.1097/AJP.0000000000000098
Johnson, B. T., & Huedo-Medina, T. B. (2013). Meta-analytic statistical inferences for continuous measre outcomes as a function of effect size metric and other assumptions.
Kaneko, K., Kawai, S., Taguchi, T., Fuchigami, Y., Yonemura, H., & Fujimoto, H. (1998). Cortical motor neuron excitability during cutaneous silent period. Electroencephalogr Clin Neurophysiol - Electromyogr Mot Control, 109, 364-368. https://doi.org/10.1016/S0924-980X(98)00031-9
Kmet, L. M., Lee, R. C., & Cook, L. S. (2004). Standard quality assessment criteria for evaluating primary research papers from a variety of fields. Alberta Heritage Foundation for Medical Research.
Kofler, M., Fuhr, P., Leis, A. A., Glocker, F. X., Kronenberg, M. F., Wissel, J., & Stetkarova, I. (2001). Modulation of upper extremity motor evoked potentials by cutaneous afferents in humans. Clinical Neurophysiology, 112, 1053-1063. https://doi.org/10.1016/S1388-2457(01)00540-5
Kofler, M., Glocker, F. X., Leis, A. A., Seifert, C., Wissel, J., Kronenberg, M. F., & Fuhr, P. (1998). Modulation of upper extremity motoneurone excitability following noxious finger tip stimulation in man: A study with transcranial magnetic stimulation. Neuroscience Letters, 246, 97-100. https://doi.org/10.1016/S0304-3940(98)00243-2
Kofler, M., Valls-Sole, J., Fuhr, P., Schindler, C., Zaccaria, B. R., & Saltuari, L. (2008). Sensory modulation of voluntary and TMS-induced activation in hand muscles. Experimental Brain Research, 188, 399-409. https://doi.org/10.1007/s00221-008-1372-2
Koo, T. K., & Li, M. Y. (2016). A guideline of selecting and reporting intraclass correlation coefficients for reliability research. Journal of Chiropractic Medicine, 15, 155-163. https://doi.org/10.1016/j.jcm.2016.02.012
Landis, J. R., & Koch, G. G. (1977). The Measurement of observer agreement for categorical data. Biometrics, 33, 159. https://doi.org/10.2307/2529310
Larsen, D. B., Graven-Nielsen, T., & Boudreau, S. A. (2019). Pain-induced reduction in corticomotor excitability is counteracted by combined action-observation and motor imagery. The Journal of Pain, 20, 1307-1316. https://doi.org/10.1016/j.jpain.2019.05.001
Larsen, D. B., Graven-Nielsen, T., Hirata, R. P., & Boudreau, S. A. (2018). Differential corticomotor excitability responses to hypertonic saline-induced muscle pain in forearm and hand muscles. Neural Plasticity, 2018, 7589601. https://doi.org/10.1155/2018/7589601
Larsen, D. B., Graven-Nielsen, T., Hirata, R. P., Seminowicz, D., Schabrun, S., & Boudreau, S. A. (2019). Corticomotor excitability reduction induced by experimental pain remains unaffected by performing a working memory task as compared to staying at rest. Experimental Brain Research, 237, 2205-2215. https://doi.org/10.1007/s00221-019-05587-y
Le Pera, D., Graven-Nielsen, T., Valeriani, M., Oliviero, A., Di Lazzaro, V., Tonali, P. A., & Arendt-Nielsen, L. (2001). Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clinical Neurophysiology, 112, 1633-1641.
Lenoir, C., Huang, G., Vandermeeren, Y., Hatem, S. M., & Mouraux, A. (2017). Human primary somatosensory cortex is differentially involved in vibrotaction and nociception. Journal of Neurophysiology, 118, 317-330. https://doi.org/10.1152/jn.00615.2016
Madsen, C. S., Finnerup, N. B., & Baumgärtner, U. (2014). Assessment of small fibers using evoked potentials. Scandinavian Journal of Pain, 5, 111-118. https://doi.org/10.1016/j.sjpain.2013.11.007
Martin, P. G., Weerakkody, N., Gandevia, S. C., & Taylor, J. L. (2008). Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. Journal of Physiology, 586, 1277-1289. https://doi.org/10.1113/jphysiol.2007.140426
Massé-Alarie, H., Beaulieu, L. D., Preuss, R., & Schneider, C. (2016). Corticomotor control of lumbar multifidus muscles is impaired in chronic low back pain: Concurrent evidence from ultrasound imaging and double-pulse transcranial magnetic stimulation. Experimental Brain Research, 234, 1033-1045. https://doi.org/10.1007/s00221-015-4528-x
Massé-Alarie, H., Salomoni, S. E., & Hodges, P. W. (2019). The nociceptive withdrawal reflex of the trunk is organized with unique muscle receptive fields and motor strategies. European Journal of Neuroscience, 50, 1932-1947. https://doi.org/10.1111/ejn.14369
Mercier, C., & Leonard, G. (2011). Interactions between pain and the motor cortex: Insights from research on phantom limb pain and complex regional pain syndrome. Physiotherapy Canada, 63, 305-314. https://doi.org/10.3138/ptc.2010-08p
Mercier, C., Roosink, M., Bouffard, J., & Bouyer, L. J. (2017). Promoting gait recovery and limiting neuropathic pain after spinal cord injury. Neurorehabil Neural Repair, 31, 315-322. https://doi.org/10.1177/1545968316680491
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & PRISMA Group. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med, 6, e1000097.
Mørch, C. D., Andersen, O. K., Graven-Nielsen, T., & Arendt-Nielsen, L. (2007). Nociceptive withdrawal reflexes evoked by uniform-temperature laser heat stimulation of large skin areas in humans. Journal of Neuroscience Methods, 160, 85-92.
Mouraux, A., Iannetti, G. D., & Plaghki, L. (2010). Low intensity intra-epidermal electrical stimulation can activate Aδ-nociceptors selectively. Pain, 150, 199-207.
Naro, A., Leo, A., Russo, M., Quartarone, A., Bramanti, P., & Calabro, R. S. (2015). Shaping thalamo-cortical plasticity: A marker of cortical pain integration in patients with post-anoxic unresponsive wakefulness syndrome? Brain Stimulation, 8, 97-104.
Nijs, J., Daenen, L., Cras, P., Struyf, F., Roussel, N., & Oostendorp, R. A. B. (2012). Nociception affects motor output: A review on sensory-motor interaction with focus on clinical implications. Clinical Journal of Pain, 28, 175-181.
Penfield, W., & Boldrey, E. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 60, 389-443.
Plichta, S. B., & Kelvin, E. A. (2011). Munro’s statistical methods for health care research, 6th ed. Wolters Kluwer Health/Lippincott Williams & Wilkins.
R Development Core Team 3.6.2. (2019). A language and environment for statistical computing. R Found Stat Comput 2. Retrieved from https://www.R-project.org
Rice, D. A., Graven-Nielsen, T., Lewis, G. N., McNair, P. J., & Dalbeth, N. (2015). The effects of experimental knee pain on lower limb corticospinal and motor cortex excitability. Arthritis Research & Therapy, 17, https://doi.org/10.1186/s13075-015-0724-0
Rittig-Rasmussen, B., Kasch, H., Fuglsang-Frederiksen, A., Svensson, P., & Jensen, T. S. (2014). The role of neuroplasticity in experimental neck pain: A study of potential mechanisms impeding clinical outcomes of training. Manual Therapy, 19, 288-293. https://doi.org/10.1016/j.math.2014.04.010
Romaniello, A., Cruccu, G., McMillan, A. S., Arendt-Nielsen, L., & Svensson, P. (2000). Effect of experimental pain from trigeminal muscle and skin on motor cortex excitability in humans. Brain Research, 882, 120-127. https://doi.org/10.1016/S0006-8993(00)02856-0
Salerno, A., Thomas, E., Olive, P., Blotman, F., Picot, M. C., & Georgesco, M. (2000). Motor cortical dysfunction disclosed by single and double magnetic stimulation in patients with fibromyalgia. Clinical Neurophysiology, 111, 994-1001. https://doi.org/10.1016/S1388-2457(00)00267-4
Salo, K.-S.-T., Vaalto, S. M. I., Koponen, L. M., Nieminen, J. O., & Ilmoniemi, R. J. (2019). The effect of experimental pain on short-interval intracortical inhibition with multi-locus transcranial magnetic stimulation. Experimental Brain Research, 237, 1503-1510. https://doi.org/10.1007/s00221-019-05502-5
Saragiotto, B., Maher, C., Yamato, T., Costa, L., Menezes Costa, L., Ostelo, R., & Macedo, L. (2016). Motor control exercise for chronic non-specific low-back pain. Cochrane Database of Systematic Reviews, https://doi.org/10.1002/14651858.CD012004
Schabrun, S. M., Burns, E., & Hodges, P. W. (2015). New insight into the time-course of motor and sensory system changes in pain. PLoS One, 10, e0142857. https://doi.org/10.1371/journal.pone.0142857
Schabrun, S. M., & Hodges, P. W. (2012). Muscle pain differentially modulates short interval intracortical inhibition and intracortical facilitation in primary motor cortex. The Journal of Pain, 13, 187-194. https://doi.org/10.1016/j.jpain.2011.10.013
Schabrun, S. M., Jones, E., Kloster, J., & Hodges, P. W. (2013). Temporal association between changes in primary sensory cortex and corticomotor output during muscle pain. Neuroscience, 235, 159-164. https://doi.org/10.1016/j.neuroscience.2012.12.072
Schabrun, S. M., Palsson, T. S., Thapa, T., & Graven-Nielsen, T. (2017). Movement does not promote recovery of motor output following acute experimental muscle pain. Pain Medicine, 19, 608-614. https://doi.org/10.1093/pm/pnx099
Suppa, A., Biasiotta, A., Belvisi, D., Marsili, L., La Cesa, S., Truini, A., Cruccu, G., & Berardelli, A. (2013). Heat-evoked experimental pain induces long-term potentiation-like plasticity in human primary motor cortex. Cerebral Cortex, 23, 1942-1951. https://doi.org/10.1093/cercor/bhs182
Svensson, P., Miles, T. S., McKay, D., & Ridding, M. C. (2003). Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation. European Journal of Pain, 7, 55-62. https://doi.org/10.1016/S1090-3801(02)00050-2
Tamburin, S., Fiaschi, A., Andreoli, A., Marani, S., & Zanette, G. (2005). Sensorimotor integration to cutaneous afferents in humans: The effect of the size of the receptive field. Experimental Brain Research, 167, 362-369. https://doi.org/10.1007/s00221-005-0041-y
Tamburin, S., Manganotti, P., Zanette, G., & Fiaschi, A. (2001). Cutaneomotor integration in human hand motor areas: somatotopic effect and interaction of afferents. Experimental Brain Research, 141, 232-241. https://doi.org/10.1007/s002210100859
Traverse, É., Brun, C., Harnois, É., & Mercier, C. (2020). Impact of experimental tonic pain on corrective motor responses to mechanical perturbations. Neural Plasticity, 2020.
Tsao, H., Tucker, K. J., & Hodges, P. W. (2011). Changes in excitability of corticomotor inputs to the trunk muscles during experimentally-induced acute low back pain. Neuroscience, 181, 127-133. https://doi.org/10.1016/j.neuroscience.2011.02.033
Urban, P. P., Solinski, M., Best, C., Rolke, R., Hopf, H. C., & Dieterich, M. (2004). Different short-term modulation of cortical motor output to distal and proximal upper-limb muscles during painful sensory nerve stimulation. Muscle and Nerve, 29, 663-669. https://doi.org/10.1002/mus.20011
Valeriani, M., Restuccia, D., Di Lazzaro, V., Oliviero, A., Le Pera, D., Profice, P., Saturno, E., & Tonali, P. (2001). Inhibition of biceps brachii muscle motor area by painful heat stimulation of the skin. Experimental Brain Research, 139, 168-172. https://doi.org/10.1007/s002210100753
Valeriani, M., Restuccia, D., Di Lazzaro, V., Oliviero, A., Profice, P., Le Pera, D., Saturno, E., & Tonali, P. (1999). Inhibition of the human primary motor area by painful heat stimulation of the skin. Clinical Neurophysiology, 110, 1475-1480. https://doi.org/10.1016/S1388-2457(99)00075-9
van Tulder, M., Furlan, A., Bombardier, C., & Bouter, L. (2003). Updated method guidelines for systematic reviews in the cochrane collaboration back review group. Spine, 28(12), 1290-1299.
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36, 1-48.
Wongpakaran, N., Wongpakaran, T., Wedding, D., & Gwet, K. L. (2013). A comparison of Cohen’s Kappa and Gwet’s AC1 when calculating inter-rater reliability coefficients: A study conducted with personality disorder samples. BMC Medical Research Methodology, 13, 1-7. https://doi.org/10.1186/1471-2288-13-61
Zhang, Y., Boudreau, S., Wang, M., Wang, K., Sessle, B., Arendt-Nielsen, L., & Svensson, P. (2010). Effects of periodontal afferent inputs on corticomotor excitability in humans. Journal of Oral Rehabilitation, 37, 39-47. https://doi.org/10.1111/j.1365-2842.2009.02016.x