Advertisement

Experimental Hand and Knee Pain Cause Differential Effects on Corticomotor Excitability

Published:February 03, 2021DOI:https://doi.org/10.1016/j.jpain.2021.01.006

      Highlights

      • Experimental pain had opposite effects on corticomotor excitability in hand and knee.
      • Effects in target muscles did not persist beyond period of pain.
      • Hand pain elicited a remote increase in corticomotor excitability in a knee muscle.
      • No effect of knee pain on corticomotor excitability in a hand muscle.

      Abstract

      Acute pain elicits a well-known inhibitory effect on upper limb corticomotor excitability, whereas the temporal effects of lower-limb experimental pain and pain in a remote limb are less clear. The aim of this study was to compare the temporal corticomotor excitability changes in the upper and lower limbs in response to acute upper and lower limb pain. In a cross-over design, 13 participants (age 29 ± 9 years; 12 male) attended 2 sessions where experimental pain was induced by injecting hypertonic saline into either the first dorsal interosseous (FDI) muscle or infrapatellar fat pad at the knee, inducing a short-lasting pain experience scored on a numerical rating scale (NRS). Motor evoked potentials (MEPs) in response to transcranial magnetic stimulation were recorded in the FDI and vastus lateralis (VL) muscles before, during, and following pain. Hand and knee pain NRS scores were not significantly different. Hand pain elicited a short duration inhibition of the FDI MEPs (P < .0001) together with a facilitation of VL MEPs (P = .001) that outlasted the duration of pain. Knee pain elicited a short-duration facilitation of VL MEPs (P = .003) with no significant effect in the FDI MEPs (P = .46). The findings indicate a limb-specific corticomotor response to experimental pain that may be related to limb function.

      Perspective

      These data demonstrate the impact of acute, experimental pain on corticomotor excitability in the upper and lower limbs. This facilitates our understanding of the effect of pain on motor control of both local and distant muscles.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to The Journal of Pain
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bank PJ
        • Peper CE
        • Marinus J
        • Beek PJ
        • van Hilten JJ
        Motor consequences of experimentally induced limb pain: A systematic review.
        Eur J Pain. 2013; 17: 145-157
        • Bennell KL
        • Hodges PW
        • Mellor R
        • Bexander C
        • Souvlis T
        The nature of anterior knee pain following injection of hypertonic saline into the infrapatellar fat pad.
        J Orthop Res. 2004; 22: 116-121
        • Billot M
        • Neige C
        • Gagné M
        • Mercier C
        • Bouyer LJ
        Effect of cutaneous heat pain on corticospinal excitability of the tibialis anterior at rest and during submaximal contraction.
        Neural Plast. 2018; (2018)8713218
        • Brouwer B
        • Ashby P
        Corticospinal projections to upper and lower limb spinal motoneurons in man.
        Electroencephalogr Clin Neurophysiol. 1990; 76: 509-519
        • Burns E
        • Chipchase LS
        • Schabrun SM
        Primary sensory and motor cortex function in response to acute muscle pain: A systematic review and meta-analysis.
        Eur J Pain. 2016; 20: 1203-1213
        • Burns E
        • Chipchase LS
        • Schabrun SM
        Reduced short- and long-latency afferent inhibition following acute muscle pain: A potential role in the recovery of motor output.
        Pain Med. 2016; 17: 1343-1352
        • Chang W-J
        • O'Connell NE
        • Beckenkamp PR
        • Alhassani G
        • Liston MB
        • Schabrun SM
        Altered primary motor cortex structure, organization, and function in chronic pain: A systematic review and meta-analysis.
        J Pain. 2018; 19: 341-359
        • Cheong JY
        • Yoon TS
        • Lee SJ
        Evaluations of inhibitory effect on the motor cortex by cutaneous pain via application of capsaicin.
        Electromyogr Clin Neurophysiol. 2003; 43: 203-210
        • Edgley SA
        • Jankowska E
        An interneuronal relay for group I and II muscle afferents in the midlumbar segments of the cat spinal cord.
        J Physiol. 1987; 389: 647-674
        • Farina S
        • Valeriani M
        • Rosso T
        • Aglioti S
        • Tamburin S
        • Fiaschi A
        • Tinazzi M
        Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation.
        Neurosci Lett. 2001; 314: 97-101
        • Gallina A
        • Salomoni SE
        • Hall LM
        • Tucker K
        • Garland SJ
        • Hodges PW
        Location-specific responses to nociceptive input support the purposeful nature of motor adaptation to pain.
        Pain. 2018; 159: 2192-2200
        • Graven-Nielsen T
        • Arendt-Nielsen L
        • Svensson P
        Staehelin Jensen T: Stimulus–response functions in areas with experimentally induced referred muscle pain — A psychophysical study.
        Brain Res. 1997; 744: 121-128
        • Graven-Nielsen T
        • Aspegren Kendall S
        • Henriksson KG
        • Bengtsson M
        • Sörensen J
        • Johnson A
        • Gerdle B
        Arendt-Nielsen L: Ketamine reduces muscle pain, temporal summation, and referred pain in fibromyalgia patients.
        Pain. 2000; 85: 483-491
        • Henriksen M
        • Rosager S
        • Aaboe J
        • Graven-Nielsen T
        • Bliddal H
        Experimental knee pain reduces muscle strength.
        J Pain. 2011; 12: 460-467
        • Hodges PW
        • Tucker K
        Moving differently in pain: A new theory to explain the adaptation to pain.
        Pain. 2011; 152: S90-S98
        • Hopkins WG
        • Marshall SW
        • Batterham AM
        • Hanin J
        Progressive statistics for studies in sports medicine and exercise science.
        Med Sci Sports Exerc. 2009; 41: 3-13
        • Iglesias C
        • Nielsen JB
        • Marchand-Pauvert V
        Corticospinal inhibition of transmission in propriospinal-like neurones during human walking.
        Eur J Neurosci. 2008; 28: 1351-1361
        • Kofler M
        • Valls-Sole J
        • Fuhr P
        • Schindler C
        • Zaccaria BR
        • Saltuari L
        Sensory modulation of voluntary and TMS-induced activation in hand muscles.
        Exp Brain Res. 2008; 188: 399-409
        • Larsen DB
        • Graven-Nielsen T
        • Hirata RP
        • Boudreau SA
        Differential corticomotor excitability responses to hypertonic saline-induced muscle pain in forearm and hand muscles.
        Neural Plast. 2018; 20187589601
        • Le Pera D
        • Graven-Nielsen T
        • Valeriani M
        • Oliviero A
        • Di Lazzaro V
        • Tonali PA
        Arendt-Nielsen L: Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain.
        Clin Neurophysiol. 2001; 112: 1633-1641
        • Lund JP
        • Donga R
        • Widmer CG
        • Stohler CS
        The pain-adaptation model: A discussion of the relationship between chronic musculoskeletal pain and motor activity.
        Can J Physiol Pharmacol. 1991; 69: 683-694
        • Marchand-Pauvert V
        • Simonetta-Moreau M
        • Pierrot-Deseilligny E
        Cortical control of spinal pathways mediating group II excitation to human thigh motoneurones.
        J Physiol. 1999; 517: 301-313
        • Martin PG
        • Weerakkody N
        • Gandevia SC
        • Taylor JL
        Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans.
        J Physiol. 2008; 586: 1277-1289
        • Park J
        • Hopkins JT
        Induced anterior knee pain immediately reduces involuntary and voluntary quadriceps activation.
        Clin J Sport Med. 2013; 23: 19-24
        • Rice DA
        • Graven-Nielsen T
        • Lewis GN
        • McNair PJ
        • Dalbeth N
        The effects of experimental knee pain on lower limb corticospinal and motor cortex excitability.
        Arthritis Res Ther. 2015; 17: 204
        • Rice DA
        • McNair PJ
        • Lewis GN
        • Mannion J
        Experimental knee pain impairs submaximal force steadiness in isometric, eccentric, and concentric muscle actions.
        Arthritis Res Ther. 2015; 17: 259
        • Rossini PM
        • Barker AT
        • Berardelli A
        • Caramia MD
        • Caruso G
        • Cracco RQ
        • Dimitrijevic MR
        • Hallett M
        • Katayama Y
        • Lucking CH
        • Marsden CD
        • Murray NMF
        • Rothwell JC
        • Swash M
        • Tomberg C
        Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: Basic principles and procedures for routine clinical application. Report of an IFCN committee.
        Electroencephalogr Clin Neurophysiol. 1994; 91: 79-92
        • Schabrun SM
        • Burns E
        • Hodges PW
        New insight into the time-course of motor and sensory system changes in pain.
        PLoS ONE. 2015; 10 (e0142857-e0142857)
        • Schabrun SM
        • Christensen SW
        • Mrachacz-Kersting N
        • Graven-Nielsen T
        Motor cortex reorganization and impaired function in the transition to sustained muscle pain.
        Cereb Cortex. 2016; 26: 1878-1890
        • Schabrun SM
        • Hodges PW
        Muscle pain differentially modulates short interval intracortical inhibition and intracortical facilitation in primary motor cortex.
        J Pain. 2012; 13: 187-194
        • Schabrun SM
        • Jones E
        • Kloster J
        • Hodges PW
        Temporal association between changes in primary sensory cortex and corticomotor output during muscle pain.
        Neuroscience. 2013; 235: 159-164
        • Schabrun SM
        • Palsson TS
        • Thapa T
        • Graven-Nielsen T
        Movement does not promote recovery of motor output following acute experimental muscle pain.
        Pain Med. 2018; 19: 608-614
        • Svensson P
        • Miles TS
        • McKay D
        • Ridding MC
        Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation.
        Eur J Pain. 2003; 7: 55-62
        • Urban PP
        • Solinski M
        • Best C
        • Rolke R
        • Hopf HC
        • Dieterich M
        Different short-term modulation of cortical motor output to distal and proximal upper-limb muscles during painful sensory nerve stimulation.
        Muscle Nerve. 2004; 29: 663-669