Abstract
Acute musculoskeletal pain is associated with reductions in corticomotor output that persists even after pain resolves. Factors that contribute to corticomotor depression following acute pain are unknown. This study examined whether psychological factors, including pain catastrophising, kinesiophobia, and implicit theories of pain, were associated with corticomotor depression following acute experimental muscle pain. Forty-two healthy individuals participated. Participants completed three questionnaires: Pain Catastrophising Scale, Tampa Scale of Kinesiophobia, and Implicit Theories of Pain Scale. Acute pain was induced into the right extensor carpi radialis brevis (ECRB) muscle by injection of hypertonic saline. Corticomotor depression was assessed as a reduction in motor-evoked potentials measured from ECRB muscle in response to transcranial magnetic stimulation before, immediately after, and at 10, 20, and 30 min following pain resolution. Corticomotor depression was present at each time point relative to baseline (p < 0.001). Higher levels of kinesiophobia were associated with less corticomotor depression 10-min post pain resolution (r = 0.32, p = 0.03), but not at any other time point (p > 0.11). When corticomotor depression was compared between individuals with ‘high’ and ‘low’ kinesiophobia, a similar relationship was observed: Individuals with high compared to low kinesiophobia displayed less corticomotor depression immediately after (p = 0.02) and 10 min post pain (p = 0.02), but not at 20 or 30 min (p = 0.05 for both). No relationship was observed with any other psychological variable (p > 0.15). These data provide preliminary support for a relationship between pain-related fear of movement and corticomotor depression in response to acute pain. These findings may have implications for clinical musculoskeletal pain disorders.
Similar content being viewed by others
Availability of data and material
Data are available from the corresponding author upon reasonable request.
References
Adachi K, Murray GM, Lee J-C, Sessle BJ (2008) Noxious lingual stimulation influences the excitability of the face primary motor cerebral cortex (face MI) in the rat. J Neurophysiol 100:1234–1244
Bashir S, Perez J, Horvath JC, Pascual-Leone A (2013) Differentiation of motor cortical representation of hand muscles by navigated mapping of optimal TMS current directions in healthy subjects. J Clin Neurophysiol 30:390
Bender R, Lange S (2001) Adjusting for multiple testing—when and how? J Clin Epidemiol 54:343–349
Bergin MJ, Tucker KJ, Vicenzino B, van den Hoorn W, Hodges PW (2014) Does movement variability increase or decrease when a simple wrist task is performed during acute wrist extensor muscle pain? Eur J Appl Physiol 114:385–393. https://doi.org/10.1007/s00421-013-2777-6
Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M (1992) Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol 9:132–136
Burns KC, Isbell LM (2007) Promoting malleability is not one size fits all: priming implicit theories of intelligence as a function of self-theories. Self and Identity 6:51–63
Burns E, Chipchase LS, Schabrun SM (2016) Primary sensory and motor cortex function in response to acute muscle pain: a systematic review and meta-analysis. Eur J Pain 20:1203–1213
Butler R (2000) Making judgments about ability: the role of implicit theories of ability in moderating inferences from temporal and social comparison information. J Pers Soc Psychol 78:965–978
Cavaleri R, Schabrun SM, Chipchase LS (2018) The reliability and validity of rapid transcranial magnetic stimulation mapping. Brain Stimul 11:1291–1295. https://doi.org/10.1016/j.brs.2018.07.043
Cavaleri R, Chipchase LS, Summers SJ, Schabrun SM (2019) Repetitive transcranial magnetic stimulation of the primary motor cortex expedites recovery in the transition from acute to sustained experimental pain: a randomised, controlled study. Pain 160:2624–2633. https://doi.org/10.1097/j.pain.0000000000001656
Chang W-J, Buscemi V, Liston MB, McAuley JH, Hodges PW, Schabrun SM (2019) Sensorimotor cortical activity in acute low back pain: a cross-sectional study. J Pain 20:819–829
Chipchase L et al (2012) A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: an international consensus study. Clin Neurophysiol 123:1698–1704
Conte A, Gilio F, Iezzi E, Frasca V, Inghilleri M, Berardelli A (2007) Attention influences the excitability of cortical motor areas in healthy humans. Exp Brain Res 182:109–117
Davila-Perez P, Jannati A, Fried PJ, Cudeiro Mazaira J, Pascual-Leone A (2018) The effects of waveform and current direction on the efficacy and test-retest reliability of transcranial magnetic stimulation. Neuroscience 393:97–109. https://doi.org/10.1016/j.neuroscience.2018.09.044
Dweck CS, Chiu C-y, Hong Y-y (1995) Implicit theories and their role in judgments and reactions: a word from two perspectives. Psychol Inq 6:267–285
Elfving B, Andersson T, Grooten WJ (2007) Low levels of physical activity in back pain patients are associated with high levels of fear-avoidance beliefs and pain catastrophizing. J Physiol Res Int 12:14–24
Furman AJ et al (2019) Cerebral peak alpha frequency reflects average pain severity in a human model of sustained, musculoskeletal pain. J Neurophysiol 122:1784–1793. https://doi.org/10.1152/jn.00279.2019
George SZ, Dover GC, Fillingim RB (2007) Fear of pain influences outcomes after exercise-induced delayed onset muscle soreness at the shoulder. Clin J Pain 23:76–84
Goldsworthy MR, Hordacre B, Ridding MC (2016) Minimum number of trials required for within- and between-session reliability of TMS measures of corticospinal excitability. Neuroscience 320:205–209. https://doi.org/10.1016/j.neuroscience.2016.02.012
Greig AM, Briggs AM, Bennell KL, Hodges PW (2014) Trunk muscle activity is modified in osteoporotic vertebral fracture and thoracic kyphosis with potential consequences for vertebral health. PLoS One 9:109
Grezes J, Valabregue R, Gholipour B, Chevallier C (2014) A direct amygdala-motor pathway for emotional displays to influence action: a diffusion tensor imaging study. Hum Brain Mapp 35:5974–5983. https://doi.org/10.1002/hbm.22598
Groppa S et al (2012) A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 123:858–882
Henchoz Y, Tetreau C, Abboud J, Piche M, Descarreaux M (2013) Effects of noxious stimulation and pain expectations on neuromuscular control of the spine in patients with chronic low back pain. Spine J 13:1263–1272. https://doi.org/10.1016/j.spinee.2013.07.452
Henderson LA, Akhter R, Youssef AM, Reeves JM, Peck CC, Murray GM, Svensson P (2016) The effects of catastrophizing on central motor activity. Eur J Pain 20:639–651. https://doi.org/10.1002/ejp.781
Higgins NC, Bailey SJ, LaChapelle DL, Harman K, Hadjistavropoulos T (2015) Coping styles, pain expressiveness, and implicit theories of chronic pain. J Psychol 149:737–750. https://doi.org/10.1080/00223980.2014.977759
Hodges PW, Smeets RJ (2015) Interaction between pain, movement, and physical activity: short-term benefits, long-term consequences, and targets for treatment. Clin J Pain 31:97–107
Hodges PW, Tucker K (2011) Moving differently in pain: a new theory to explain the adaptation to pain. Pain 152:S90–S98
Hudes K (2011) The Tampa Scale of Kinesiophobia and neck pain, disability and range of motion: a narrative review of the literature. J Can Chiropr Assoc 55:222–232
Jacobs JV, Roy CL, Hitt JR, Popov RE, Henry SM (2016) Neural mechanisms and functional correlates of altered postural responses to perturbed standing balance with chronic low back pain. Neuroscience 339:511–524. https://doi.org/10.1016/j.neuroscience.2016.10.032
Karayannis NV, Smeets RJ, van den Hoorn W, Hodges PW (2013) Fear of movement is related to trunk stiffness in low back pain. PLoS One 8:e67779
Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720
Kori SH (1990) Kinisophobia: a new view of chronic pain behavior. Pain Manag 3:35–43
Larsen DB, Graven-Nielsen T, Hirata RP, Boudreau SA (2018) Differential corticomotor excitability responses to hypertonic saline-induced muscle pain in forearm and hand muscles. Neural Plast 2018:7589601. https://doi.org/10.1155/2018/7589601
Larsen DB, Graven-Nielsen T, Boudreau SA (2019a) Pain-induced reduction in corticomotor excitability is counteracted by combined action-observation and motor imagery. J Pain 08:08. https://doi.org/10.1016/j.jpain.2019.05.001
Larsen DB, Graven-Nielsen T, Hirata RP, Seminowicz D, Schabrun S, Boudreau SA (2019b) Corticomotor excitability reduction induced by experimental pain remains unaffected by performing a working memory task as compared to staying at rest. Exp Brain Res 237:2205–2215. https://doi.org/10.1007/s00221-019-05587-y
Lazzaro V et al (2001) Comparison of descending volleys evoked by monophasic and biphasic magnetic stimulation of the motor cortex in conscious humans. Exp Brain Res 141:121–127
Le Pera D, Graven-Nielsen T, Valeriani M, Oliviero A, Di Lazzaro V, Tonali PA, Arendt-Nielsen L (2001) Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 112:1633–1641
Leal PC, Goes TC, da Silva LCF, Teixeira-Silva F (2017) Trait vs. state anxiety in different threatening situations. Trends Psychiatry Psychother. 39:147–157
Leeuw M et al (2008) Exposure in vivo versus operant graded activity in chronic low back pain patients: results of a randomized controlled trial. J Pain 138:192–207
Lewis S, Holmes P, Woby S, Hindle J, Fowler N (2012) The relationships between measures of stature recovery, muscle activity and psychological factors in patients with chronic low back pain. Man Ther 17:27–33. https://doi.org/10.1016/j.math.2011.08.001
Lindstroem R, Graven-Nielsen T, Falla D (2012) Current pain and fear of pain contribute to reduced maximum voluntary contraction of neck muscles in patients with chronic neck pain. Arch Phys Med Rehabil 93:2042–2048. https://doi.org/10.1016/j.apmr.2012.04.014
Lumley MA et al (2011) Pain and emotion: a biopsychosocial review of recent research. J Clin Psychol 67:942–968. https://doi.org/10.1002/jclp.20816
Malcolm MP, Triggs WJ, Light KE, Shechtman O, Khandekar G, Gonzalez Rothi LJ (2006) Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clin Neurophysiol 117:1037–1046
Martin PG, Weerakkody N, Gandevia S, Taylor J (2008) Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol 586:1277–1289
Masse-Alarie H, Beaulieu LD, Preuss R, Schneider C (2016) Influence of chronic low back pain and fear of movement on the activation of the transversely oriented abdominal muscles during forward bending. J Electromyogr Kinesiol 27:87–94. https://doi.org/10.1016/j.jelekin.2016.02.004
McGregor KM et al (2012) Motor map reliability and aging: a TMS/fMRI study. Exp Brain Res 219:97–106
Meier ML, Stämpfli P, Vrana A, Humphreys BK, Seifritz E, Hotz-Boendermaker S (2016) Neural correlates of fear of movement in patients with chronic low back pain vs. pain-free individuals. Front Hum Neurosci 10:386. https://doi.org/10.3389/fnhum.2016.00386
Melzack R (1987) The short-form McGill pain questionnaire. Pain 30:191–197
Moseley GL, Hodges PW (2006) Reduced variability of postural strategy prevents normalization of motor changes induced by back pain: a risk factor for chronic trouble? Behav Neurosci 120:474–476. https://doi.org/10.1037/0735-7044.120.2.474
Moseley GL, Nicholas MK, Hodges PW (2004) Does anticipation of back pain predispose to back trouble? Brain 127:2339–2347
Nash PG, Macefield VG, Klineberg ÝJ, Gustin SM, Murray GM, Henderson LA (2010) Changes in human primary motor cortex activity during acute cutaneous and muscle orofacial pain. J Orofac Pain 24:379–390
Ngomo S, Leonard G, Moffet H, Mercier C (2012) Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability. J Neurosci Methods 205:65–71. https://doi.org/10.1016/j.jneumeth.2011.12.012
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Olugbade T, Bianchi-Berthouze N, Williams ACC (2019) The relationship between guarding, pain, and emotion. Pain Rep 4:e770. https://doi.org/10.1097/pr9.0000000000000770
Pakzad M, Fung J, Preuss R (2016) Pain catastrophizing and trunk muscle activation during walking in patients with chronic low back pain. Gait Posture 49:73–77. https://doi.org/10.1016/j.gaitpost.2016.06.025
Picavet HSJ, Vlaeyen JW, Schouten JS (2002) Pain catastrophizing and kinesiophobia: predictors of chronic low back pain. Am J Epidemiol 156:1028–1034
Quartana PJ, Campbell CM, Edwards RR (2009) Pain catastrophizing: a critical review. Expert Rev Neurother 9:745–758. https://doi.org/10.1586/ern.09.34
Rice DA, Graven-Nielsen T, Lewis GN, McNair PJ, Dalbeth N (2015) The effects of experimental knee pain on lower limb corticospinal and motor cortex excitability. Arthritis Res Ther 17:204. https://doi.org/10.1186/s13075-015-0724-0
Rizzo G et al (2018) The limbic and sensorimotor pathways of the human amygdala: a structural connectivity study. Neuroscience 385:166–180. https://doi.org/10.1016/j.neuroscience.2018.05.051
Romero C, Master A, Paunesku D, Dweck CS, Gross JJ (2014) Academic and emotional functioning in middle school: the role of implicit theories. Emotion 14:227–234
Ross GB, Mavor M, Brown SHM, Graham RB (2015) The effects of experimentally induced low back pain on spine rotational stiffness and local dynamic stability. Ann Biomed Eng 43:2120–2130. https://doi.org/10.1007/s10439-015-1268-9
Ross GB, Sheahan PJ, Mahoney B, Gurd BJ, Hodges PW, Graham RB (2017) Pain catastrophizing moderates changes in spinal control in response to noxiously induced low back pain. J Biomech 58:64–70
Schabrun SM, Hodges PW (2012) Muscle pain differentially modulates short interval intracortical inhibition and intracortical facilitation in primary motor cortex. J Pain 13:187–194. https://doi.org/10.1016/j.jpain.2011.10.013
Schabrun SM, Burns E, Hodges PW (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 SM, Palsson TS, Thapa T, Graven-Nielsen T (2017) Movement does not promote recovery of motor output following acute experimental muscle pain. Pain Med 19:608–614
Seminowicz DA, Davis KD (2006) Cortical responses to pain in healthy individuals depends on pain catastrophizing. Pain 120:297–306. https://doi.org/10.1016/j.pain.2005.11.008
Stefan K, Wycislo M, Classen J (2004) Modulation of associative human motor cortical plasticity by attention. J Neurophysiol 92:66–72
Sullivan MJ, Bishop SR, Pivik J (1995) The pain catastrophizing scale: development and validation. Psychol Ass 7:524
Summers SJ, Chipchase LS, Hirata R, Graven-Nielsen T, Cavaleri R, Schabrun SM (2019a) Motor adaptation varies between individuals in the transition to sustained pain. Pain 160:2115–2125. https://doi.org/10.1097/j.pain.0000000000001604
Summers SJ, Higgins NC, Te M, Byrne A, Chipchase LS (2019b) The effect of implicit theories of pain on pain and disability in people with chronic low back pain. Musculoskelet Sci Pract 40:65–71. https://doi.org/10.1016/j.msksp.2019.01.013
Svensson P, Miles TS, McKay D, Ridding MC (2003) Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation. Eur J Pain 7:55–62
Swinkels-Meewisse E, Swinkels R, Verbeek A, Vlaeyen J, Oostendorp R (2003) Psychometric properties of the Tampa Scale for kinesiophobia and the fear-avoidance beliefs questionnaire in acute low back pain. Man Ther 8:29–36
Swinkels-Meewisse IE, Roelofs J, Schouten EG, Verbeek AL, Oostendorp RA, Vlaeyen JW (2006) Fear of movement/(re) injury predicting chronic disabling low back pain: a prospective inception cohort study. Spine 31:658–664
Thomson RH, Garry MI, Summers JJ (2008) Attentional influences on short-interval intracortical inhibition. Clin Neurophysiol 119:52–62
Trost Z, France CR, Thomas JS (2011) Pain-related fear and avoidance of physical exertion following delayed-onset muscle soreness. Pain 152:1540–1547. https://doi.org/10.1016/j.pain.2011.02.038
Uddin LQ, Nomi JS, Hébert-Seropian B, Ghaziri J, Boucher O (2017) Structure and function of the human insula. J Clin Neurophysiol 34:300–306. https://doi.org/10.1097/WNP.0000000000000377
van de Ruit M, Perenboom MJ, Grey MJ (2015) TMS brain mapping in less than two minutes. Brain Stimul 8:231–239. https://doi.org/10.1016/j.brs.2014.10.020
Vlaeyen JW, Kole-Snijders AM, Boeren RG, Van Eek H (1995) Fear of movement/(re) injury in chronic low back pain and its relation to behavioral performance. Pain 62:363–372
Funding
This research did not receive any specific funding from agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no conflicts of interest.
Additional information
Communicated by Winston D. Byblow.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Summers, S.J., Chalmers, K.J., Cavaleri, R. et al. Fear of movement is associated with corticomotor depression in response to acute experimental muscle pain. Exp Brain Res 238, 1945–1955 (2020). https://doi.org/10.1007/s00221-020-05854-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-020-05854-3