Abstract
Experimental pain is known to affect neuroplasticity of the motor cortex as well as motor performance, but less is known about neuroplasticity of somatosensory processing in the presence of pain. Early somatosensory evoked potentials (SEPs) provide a mechanism for investigating alterations in sensory processing and sensorimotor integration (SMI). The overall aim of this study was to investigate the interactive effects of acute pain, motor training, and sensorimotor processing. Two groups of twelve participants (N = 24) were randomly assigned to either an intervention (capsaicin cream) or placebo (inert lotion) group. SEP amplitudes were collected by stimulation of the median nerve at baseline, post-application and post-motor training. Participants performed a motor sequence task while reaction time and accuracy data were recorded. The amplitude of the P22-N24 complex was significantly increased following motor training for both groups F(2,23) = 3.533, p < 0.05, while Friedman’s test for the P22-N30 complex showed a significant increase in the intervention group [χ 2 (df = 2, p = 0.016) = 8.2], with no significant change in the placebo group. Following motor training, reaction time was significantly decreased for both groups F(1,23) = 59.575, p < 0.01 and overall accuracy differed by group [χ 2 (df = 3, p < 0.001) = 19.86], with post hoc testing indicating that the intervention group improved in accuracy following motor training [χ 2 (df = 1, p = 0.001) = 11.77] while the placebo group had worse accuracy [χ 2 (df = 1, p = 0.006) = 7.67]. The improved performance in the presence of capsaicin provides support for the enhancement of knowledge acquisition with the presence of nontarget stimuli. In addition, the increase in SEP peak amplitudes suggests that early SEP changes are markers of SMI changes accompanying motor training and acute pain.
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References
Apps R, Garwicz M (2005) Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6(4):297–311
Boudreau S, Romaniello A, Wang K, Svensson P, Sessle BJ, Arendt-Nielsen L (2007) The effects of intra-oral pain on motor cortex neuroplasticity associated with short-term novel tongue-protrusion training in humans. Pain 132(1–2):169
Cebolla A, Palmero-Soler E, Dan B, Cheron G (2011) Frontal phasic and oscillatory generators of the N30 somatosensory evoked potential. NeuroImage 54(2):1297–1306
Cheron G, Borenstein S (1987) Specific gating of the early somatosensory evoked potentials during active movement. Electroencephalogr Clin Neurophysiol 67(6):537–548
Cheron G, Borenstein S (1991) Gating of the early components of the frontal and parietal somatosensory evoked potentials in different sensory-motor interference modalities. Electroencephalogr Clini Neurophysiol 80(6):522–530
Conner JM, Culberson A, Packowski C, Chiba AA, Tuszynski MH (2003) Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 38(5):819–829
Cruccu G, Aminoff M, Curio G, Guerit J, Kakigi R, Mauguiere F, Rossini P, Treede R, Garcia-Larrea L (2008) Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol 119(8):1705–1719
Dolphin NW, Crue BL Jr (1989) Pain: clinical manual for nursing practice. Clin J Pain 5(4):363
Dostrovsky JO, Guilbaud G (1990) Nociceptive responses in medial thalamus of the normal and arthritic rat. Pain 40(1):93–104
Doyon J, Ungerleider LG (2002) Functional anatomy of motor skill learning. In: Squire L, Schacter D (eds) Neuropsychology of memory, 3rd edn. Guilford Press, New York, pp 225–238
Ferguson A, Crown E, Grau J (2006) Nociceptive plasticity inhibits adaptive learning in the spinal cord. Neuroscience 141(1):421–431
Flor H (2003) Cortical reorganisation and chronic pain: implications for rehabilitation. J Rehabil Med 41:66–72
Friston K, Frith C, Passingham R, Liddle P, Frackowiak R (1992) Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study. Biol Sci 248(1323):223–228
Fujii M, Yamada T, Aihara M, Kokubun Y, Noguchi Y, Matsubara M, Malcolm H (1994) The effects of stimulus rates upon median, ulnar and radial nerve somatosensory evoked potentials. Electroencephalogr Clin Neurophysiol 92(6):518–526
Gao JH, Parsons LM, Bower JM, Xiong J, Li J, Fox PT (1996) Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272(5261):545–547
Grafton ST, Mazziotta JC, Presty S, Friston KJ, Frackowiak R, Phelps ME (1992) Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J Neurosci 12(7):2542–2548
Haavik H, Murphy B (2013) Selective changes in cerebellar-cortical processing following motor training. Exp Brain Res 231(4):397–403
Haavik Taylor H, Murphy B (2007) Altered cortical integration of dual somatosensory input following the cessation of a 20 min period of repetitive muscle activity. Exp Brain Res 178(4):488–498
Haavik Taylor H, Murphy B (2010) Altered central integration of dual somatosensory input after cervical spine manipulation. J Manip Physiol Ther 33(3):178–188
Hazeltine E, Grafton ST, Ivry R (1997) Attention and stimulus characteristics determine the locus of motor-sequence encoding: A PET study. Brain 120(1):123–140
Hluštík P, Solodkin A, Noll DC, Small SL (2004) Cortical plasticity during three-week motor skill learning. J Clin Neurophysiol 21(3):180–191
Hodges PW, Moseley GL (2003) Pain and motor control of the lumbopelvic region: effect and possible mechanisms. J Electromyogr Kinesiol 13(4):361–370
Hook MA, Huie JR, Grau JW (2008) Peripheral inflammation undermines the plasticity of the isolated spinal cord. Behav Neurosci 122(1):233
Iadarola MJ, Berman KF, Zeffiro TA, Byas-Smith MG, Gracely RH, Max MB, Bennett GJ (1998) Neural activation during acute capsaicin-evoked pain and allodynia assessed with PET. Brain 121(5):931–947
Jenkins I, Brooks D, Nixon P, Frackowiak R, Passingham R (1994) Motor sequence learning: a study with positron emission tomography. J Neurosci 14(6):3775–3790
Jueptner M, Weiller C (1998) A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121(8):1437–1449
Kanovsky P, Bares M, Rektor I (2003) The selective gating of the N30 cortical component of the somatosensory evoked potentials of median nerve is different in the mesial and dorsolateral frontal cortex: evidence from intracerebral recordings. Clin Neurophysiol 114(6):981–991
Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci 95(3):861–868
Kelso JS (1992) Theoretical concepts and strategies for understanding perceptual-motor skill: from information capacity in closed systems to self-organization in open, nonequilibrium systems. J Exp Psychol Gen 121(3):260
Knecht S, Sörös P, Gürtler S, Imai T, Ringelstein E, Henningsen H (1998) Phantom sensations following acute pain. Pain 77(2):209–213
Koeneke S, Lutz K, Herwig U, Ziemann U, Jäncke L (2006) Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability. Exp Brain Res 174(2):199–209
Maihöfner C, Handwerker HO, Neundörfer B, Birklein F (2003) Patterns of cortical reorganization in complex regional pain syndrome. Neurology 61(12):1707–1715
Maihöfner C, Jesberger F, Seifert F, Kaltenhäuser M (2010) Cortical processing of mechanical hyperalgesia: a MEG study. Eur J Pain 14(1):64–70
Manto M, Bastian AJ (2007) Cerebellum and the deciphering of motor coding. Cerebellum 6:3–6
Mauguiere F (1999) Somatosensory evoked potentials: normal responses, abnormal waveforms and clinical applications in neurological diseases. In: Niedermeyer E (ed) Electroencephalography: basic principles, clinical applications, and related fields. Williams and Wilkins, Baltimore
Mauguiere F, Allison T, Babiloni C, Buchner H, Eisen A, Goodin D, Jones S, Kakigi R, Matsuoka S, Nuwer M (1999) Somatosensory evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 52:79–90
McGaughy J, Dalley J, Morrison C, Everitt B, Robbins T (2002) Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J Neurosci 22(5):1905–1913
Molinari M, Leggio M, Thaut M (2007) The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain. Cerebellum 6(1):18–23
Molinari M, Restuccia D, Leggio MG (2009) State estimation, response prediction, and cerebellar sensory processing for behavioral control. Cerebellum 8(3):399–402
Murphy B, Taylor H, Wilson S, Oliphant G, Mathers K (2003) Rapid reversible changes to multiple levels of the human somatosensory system following the cessation of repetitive contractions: a somatosensory evoked potential study. Clin Neurophysiol 114(8):1531–1537
Neugebauer V, Li W (2003) Differential sensitization of amygdala neurons to afferent inputs in a model of arthritic pain. J Neurophysiol 89(2):716–727
Nissen MJ, Knopman DS, Schacter DL (1987) Neurochemical dissociation of memory systems. Neurology 37(5):789
Nuwer MR, Aminoff M, Desmedt J, Eisen AA, Goodin D, Matsuoka S, Mauguière F, Shibasaki H, Sutherling W, Vibert JF (1994) IFCN recommended standards for short latency somatosensory evoked potentials. Report of an IFCN committee. International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 91(1):6
Pascual-Leone A, Torres F (1993) Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain 116:39–52
Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74(3):1037–1045
Passmore SR, Bosse J, Murphy B, Lee TD (2014) The impact and specificity of nerve pertubation on novel vibrotactile sensory letter learning. Somatosens Mot Res (in press)
Rosenkranz K, Rothwell JC (2004) The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex. J Physiol 561(1):307–320
Rossi S, della Volpe R, Ginanneschi F, Ulivelli M, Bartalini S, Spidalieri R, Rossi A (2003) Early somatosensory processing during tonic muscle path in humans: relation to loss of proprioception and motor ‘defensive’ strategies. Clin Neurophysiol 114(7):1351–1358
Rottmann S, Jung K, Ellrich J (2008) Electrical low-frequency stimulation induces homotopic long-term depression of nociception and pain from hand in man. Clin Neurophysiol 119(8):1895–1904
Schweinhardt P, Lee M, Tracey I (2006) Imaging pain in patients: is it meaningful? Curr Opin Neurol 19(4):392–400
Shiri R, Viikari-Juntura E, Varonen H, Heliövaara M (2006) Prevalence and determinants of lateral and medial epicondylitis: a population study. Am J Epidemiol 164(11):1065–1074
Sonoo M, Sakuta M, Shimpo T, Genba K, Mannen T (1991) Widespread N18 in median nerve SEP is preserved in a pontine lesion. Electroencephalogr Clin Neurophysiol 80(3):238–240
Sörös P, Knecht S, Bantel C, Imai T, Wüsten R, Pantev C, Lütkenhöner B, Bürkle H, Henningsen H (2001) Functional reorganization of the human primary somatosensory cortex after acute pain demonstrated by magnetoencephalography. Neurosci Lett 298(3):195–198
Stefan K, Wycislo M, Classen J (2004) Modulation of associative human motor cortical plasticity by attention. J Neurophysiol 92(1):66–72
Streiner GRNDL (2008) Biostatistics: the bare essentials. 3rd edn. McGraw-Hill Europe
Svensson P, Romaniello A, Arendt-Nielsen L, Sessle BJ (2003) Plasticity in corticomotor control of the human tongue musculature induced by tongue-task training. Exp Brain Res 152(1):42–51
Svensson P, Romaniello A, Wang K, Arendt-Nielsen L, Sessle B (2006) One hour of tongue-task training is associated with plasticity in corticomotor control of the human tongue musculature. Exp Brain Res 173(1):165–173
Tinazzi M, Zanette G, Polo A, Volpato D, Manganotti P, Bonato C, Testoni R, Fiaschi A (1997) Transient deafferentation in humans induces rapid modulation of primary sensory cortex not associated with subcortical changes: a somatosensory evoked potential study. Neurosci Lett 223(1):21–24
Tinazzi M, Zanette G, Volpato D, Testoni R, Bonato C, Manganotti P, Miniussi C, Fiaschi A (1998) Neurophysiological evidence of neuroplasticity at multiple levels of the somatosensory system in patients with carpal tunnel syndrome. Brain 121(9):1785–1794
Tinazzi M, Fiaschi A, Rosso T, Faccioli F, Grosslercher J, Aglioti SM (2000) Neuroplastic changes related to pain occur at multiple levels of the human somatosensory system: a somatosensory-evoked potentials study in patients with cervical radicular pain. J Neurosci 20(24):9277–9283
Tinazzi M, Valeriani M, Moretto G, Rosso T, Nicolato A, Fiaschi A, Aglioti S (2004) Plastic interactions between hand and face cortical representations in patients with trigeminal neuralgia: a somatosensory-evoked potentials study. Neuroscience 127(3):769–776
Verrillo RT, Bolanowski SJ, Baran F, Smith PF (1996) Effects of underwater environmental conditions on vibrotactile thresholds. J Acoust Soc Am 100:651
Waberski TD, Buchner H, Perkuhn M, Gobbelé R, Wagner M, Kücker W, Silny J (1999) N30 and the effect of explorative finger movements: a model of the contribution of the motor cortex to early somatosensory potentials. Clin Neurophysiol 110(9):1589–1600
Wang L, Chen AC, Arendt-Nielsen L (2006) Cortical plasticity: effect of high and low intensity conditioning electrical stimulations (100 Hz) on SEPs to painful finger stimulation. Clin Neurophysiol 117(5):1075–1084
Zhang Z, Francisco EM, Holden JK, Dennis RG, Tommerdahl M (2009) The impact of non-noxious heat on tactile information processing. Brain Res 1302:97–105
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The authors would like to acknowledge the following organizations for support and funding: Natural Science and Engineering Research Council of Canada (NSERC), Canada Foundation for Innovation, Ontario Ministry of Research and Innovation, the University of Ontario Institute of Technology and Jessica Bossé for assistance with data collection.
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Dancey, E., Murphy, B., Srbely, J. et al. The effect of experimental pain on motor training performance and sensorimotor integration. Exp Brain Res 232, 2879–2889 (2014). https://doi.org/10.1007/s00221-014-3966-1
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DOI: https://doi.org/10.1007/s00221-014-3966-1