Highlights
- •Action observation and motor imagery facilitate corticomotor excitability.
- •Intramuscular pain reduces corticomotor excitability.
- •Action observation and motor imagery counterbalance pain-induced reduction in corticomotor excitability.
Abstract
Musculoskeletal pain reduces corticomotor excitability (CE) and methods modulating
such CE reduction remain elusive. This study aimed to modulate pain-induced CE reduction
by performing action observation and motor imagery (AOMI) during experimental muscle
pain. Twelve healthy participants participated in 3 cross-over and randomized sessions
separated by 1 week. During the AOMI session subjects performed an AOMI task for 10
minutes. In the AOMI+PAIN session, hypertonic saline was injected in the first dorsal
interosseous muscle before performing the AOMI task. In the PAIN session, participants
remained at rest for 10 minutes or until pain-resolve after the hypertonic saline
injection. CE was assessed using transcranial magnetic stimulation motor-evoked potentials
(TMS-MEPs) of the first dorsal interosseous muscle at baseline, during, immediately
after, and 10 minutes after AOMI and/or PAIN. Facilitated TMS-MEPs were found after
2 and 4 minutes of AOMI performance (P < .017) whereas a reduction in TMS-MEPs occurred at 4 minutes (P < .017) during the PAIN session. Performing the AOMI task during pain counteracted
the reduction in CE, as evident by no change in TMS-MEPs during the AOMI+PAIN session
(P > .017). Pain intensity was similar between the AOMI+PAIN and PAIN sessions (P = .71). This study, which may be considered a pilot, demonstrated the counteracting
effects of AOMI on pain-induced decreases in CE and warrants further studies in a
larger population.
Perspective
This is the first study to demonstrate a method counteracting the reduction in CE
associated with acute pain and advances therapeutic possibilities for individuals
with chronic musculoskeletal pain.
Keywords
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 accessOne-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 PainAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- The excitability of the human motor cortex increases during execution and mental imagination of sequential but not repetitive finger movements.Exp Brain Res. 1996; 111: 465-472
- Lateralization in motor facilitation during action observation: A TMS study.Exp Brain Res. 2002; 144: 127-131
- Excitability changes occurring in the human spinal cord while looking at video recorded hand movements.Pflugers Arch J Physiol. 1998; 435: R18
- Reliability and minimal detectable change of transcranial magnetic stimulation outcomes in healthy adults: A systematic review.Brain Stimul. 2017; 10: 196-213
- Controlling the false discovery rate: A practical and powerful approach to multiple testing.J R Stat Soc. 1995; 57: 289-300
- Exercise for chronic musculoskeletal pain: A biopsychosocial approach.Musculoskeletal Care. 2017; 15: 413-421
- The effects of intra-oral pain on motor cortex neuroplasticity associated with short-term novel tongue-protrusion training in humans.Pain. 2007; 132: 169-178
- Tonic pain experienced during locomotor training impairs retention despite normal performance during acquisition.J Neurosci. 2014; 34: 9190-9195
- Inhibition or facilitation? Modulation of corticospinal excitability during motor imagery.Neuropsychologia. 2018; 111: 360-368
- Action observation activates premotor and parietal areas in a somatotopic manner: An fMRI study.Eur J Neurosci. 2001; 13: 400-404
- Motor imagery beyond the joint limits: A transcranial magnetic stimulation study.Biol Psychol. 2010; 85: 283-290
- 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
- Unilateral practice of a ballistic movement causes bilateral increases in performance and corticospinal excitability.J Appl Physiol. 2008; 104: 1656-1664
- ALE meta-analysis of action observation and imitation in the human brain.Neuroimage. 2010; 50: 1148-1167
- A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: An international consensus study.Clin Neurophysiol. 2012; 123: 1698-1704
- Modulation of motor cortex inhibition during motor imagery.J Neurophysiol. 2017; 117: 1776-1784
- Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans.Neuroimage. 2001; 14: 1444-1453
- Individual differences in the subjective experience of pain: New insights into mechanisms and models.Headache J Head Face Pain. 2010; 50: 1531-1535
- Motor imagery during action observation: A brief review of evidence, theory and future research opportunities.Front Neurosci. 2016; 10: 1-10
- Motor facilitation during action observation: A magnetic stimulation study.J Neurophysiol. 1995; 73: 2608-2611
- Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation.Neurosci Lett. 2001; 314: 97-101
- Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery.Neuroimage. 2007; 37: 1315-1328
- Corticospinal facilitation during first and third person imagery.Exp Brain Res. 2006; 168: 143-151
- Clinical relevance of action observation in upper-limb stroke rehabilitation: A possible role in recovery of functional dexterity. A randomized clinical trial.Neurorehabil Neural Repair. 2012; 26: 456-462
- Changes in motor cortex excitability following training of a novel goal-directed motor task.Eur J Appl Physiol. 2009; 105: 47-54
- Action recognition in the premotor cortex.Brain. 1996; 119: 593-609
- Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex.Neurology. 2001; 57: 449-455
- Assessment of mechanisms in localized and widespread musculoskeletal pain.Nat Rev Rheumatol. 2010; 6: 599-606
- Stimulus-response functions in areas with experimentally induced referred muscle pain - A psychophysical study.Brain Res. 1997; 744: 121-128
- Selecting a sample size for studies with repeated measures.BMC Med Res Methodol. 2013; 13: 100
- Moving differently in pain: A new theory to explain the adaptation to pain.Pain. 2011; 152: S90-S98
- Neural simulation of action: A unifying mechanism for motor cognition.Neuroimage. 2001; 14: 103-109
- Resonance of cortico-cortical connections of the motor system with the observation of goal directed grasping movements.Neuropsychologia. 2010; 48: 3513-3520
- Effect of tonic pain on motor acquisition and retention while learning to reach in a force field.PLoS One. 2014; 9: e99159
- Differential corticomotor excitability responses to hypertonic saline-induced muscle pain in forearm and hand muscles.Neural Plast. 2018; 2018
- Reliability of transcranial magnetic stimulation induced corticomotor excitability measurements for a hand muscle in healthy and chronic stroke subjects.J Neurol Sci. 2014; 341: 105-109
- The efficacy of pain neuroscience education on musculoskeletal pain: A systematic review of the literature.Physiother Theory Pract. 2016; 32: 332-355
- Reliability of motor cortex transcranial magnetic stimulation in four muscle representations.Clin Neurophysiol. 2006; 117: 1037-1046
- Pain-related suppression of beta oscillations facilitates voluntary movement.Cereb Cortex. 2017; 27: 2592-2606
- Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex.J Physiol. 2004; 561: 331-338
- Role of the human motor cortex in rapid motor learning.Exp Brain Res. 2001; 136: 431-438
- Effect of movement-related pain on behaviour and corticospinal excitability changes associated with arm movement preparation.J Physiol. 2018; 596: 2917-2929
- Excitability changes in the human primary motor cortex during observation with motor imagery of chopstick use.J Phys Ther Sci. 2011; 23: 703-706
- The assessment and analysis of handedness: The Edinburgh inventory.Neuropsychologia. 1971; 9: 97-113
- Is neuroplasticity in the central nervous system the missing link to our understanding of chronic musculoskeletal disorders?.BMC Musculoskelet Disord. 2015; 16: 25
- Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain.Clin Neurophysiol. 2001; 112: 1633-1641
- Ipsilateral involvement of primary motor cortex during motor imagery.Eur J Neurosci. 2000; 12: 3059-3063
- Primary motor and sensory cortex activation during motor performance and motor imagery: A functional magnetic resonance imaging study.J Neurosci. 1996; 16: 7688-7698
- The influence of pain on motor preparation in the human brain.J Neurophysiol. 2017; 118: 2267-2274
- Shaping the excitability of human motor cortex with premotor rTMS.J Physiol. 2004; 554: 483-495
- Premotor cortex and the recognition of motor actions.Cogn Brain Res. 1996; 3: 131-141
- Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research.Clin Neurophysiol. 2009; 120: 2008-2039
- Screening questionnaire before TMS: An update.Clin Neurophysiol. 2011; 122: 1686
- Corticospinal excitability modulation to hand muscles during movement imagery.Cereb Cortex. 1999; 9: 161-167
- Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee.Clin Neurophysiol. 2015; 126: 1071-1107
- New insight into the time-course of motor and sensory system changes in pain.PLoS One. 2015; 10e0142857
- Smudging of the motor cortex is related to the severity of low back pain.Spine (Phila Pa 1976). 2017; 42: 1172-1178
- Muscle pain differentially modulates short interval intracortical inhibition and intracortical facilitation in primary motor cortex.J Pain. 2012; 13: 187-194
- Movement does not promote recovery of motor output following acute experimental muscle pain.Pain Med. 2017; : 1-7
- Interactions of pain intensity and cognitive load: The brain stays on task.Cereb Cortex. 2007; 17: 1412-1422
- Lateralization of unimanual and bimanual motor imagery.Brain Res. 2006; 1095: 139-147
- Modulation of cortical excitability during action observation: A transcranial magnetic stimulation study.Neuroreport. 2000; 11: 2289-2292
- Improving motor imagery practice with synchronous action observation in stroke patients.Top Stroke Rehabil. 2016; 23: 245-253
- Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation.Eur J Pain. 2003; 7: 55-62
- Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: Segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex.Exp Brain Res. 1998; 120: 114-128
- Input organization of the distal and proximal forelimb areas in the monkey primary motor cortex: A retrograde labeling study.J Comp Neurol. 1993; 333: 199-209
- ISSLS Prize Winner: Smudging the motor brain in young adults with recurrent low back pain.Spine (Phila Pa 1976). 2011; 36: 1721-1727
- Inhibition of biceps brachii muscle motor area by painful heat stimulation of the skin.Exp Brain Res. 2001; 139: 168-172
- Inhibition of the human primary motor area by painful heat stimulation of the skin 135.Clin Neurophysiol. 1999; 110: 1475-1480
- Enhanced activation of motor execution networks using action observation combined with imagination of lower limb movements.PLoS One. 2013; 8: e72403
- Multiple roles of motor imagery during action observation.Front Hum Neurosci. 2013; 7: 1-13
- Variation in the response to transcranial magnetic brain stimulation in the general population.Clin Neurophysiol. 2002; 113: 1165-1171
- Viewing instructions accompanying action observation modulate corticospinal excitability.Front Hum Neurosci. 2016; 10: 1-10
- Combined action observation and imagery facilitates corticospinal excitability.Front Hum Neurosci. 2014; 8: 1-9
Article info
Publication history
Published online: May 08, 2019
Accepted:
May 2,
2019
Received in revised form:
March 22,
2019
Received:
January 17,
2019
Footnotes
Work was performed in laboratories at Aalborg University, 9220 Aalborg SØ, Aalborg, Denmark.
Disclosures: The authors declare no conflicts of interest. Center for Neuroplasticity and Pain (CNAP) is supported by the Danish National Research Foundation (DNRF121).
Institutional URL: http://personprofil.aau.dk/111183
Identification
Copyright
© 2019 by the American Pain Society