Fatigue-induced increase in intracortical communication between mid/anterior insular and motor cortex during cycling exercise

In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant‐load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalogr...

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Vydáno v:The European journal of neuroscience Ročník 34; číslo 12; s. 2035 - 2042
Hlavní autoři: Hilty, Lea, Langer, Nicolas, Pascual-Marqui, Roberto, Boutellier, Urs, Lutz, Kai
Médium: Journal Article
Jazyk:angličtina
Vydáno: Oxford, UK Blackwell Publishing Ltd 01.12.2011
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ISSN:0953-816X, 1460-9568, 1460-9568
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Abstract In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant‐load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact‐free periods of 1‐min duration. To quantify fatigue‐induced intracortical communication, mean intra‐hemispheric lagged phase synchronization between mid/anterior insular and motor cortex was calculated: (i) at the beginning of cycling; (ii) at the end of cycling; and (iii) during recovery cycling. Results revealed significantly increased lagged phase synchronization at the end of cycling, which returned to baseline during recovery cycling after subjects’ cessation of exercise. Following previous imaging studies reporting the mid/anterior insular cortex as an essential instance processing a variety of sensory stimuli and signalling forthcoming physiological threat, our results provide further evidence that during a fatiguing exercise this structure might not only integrate and evaluate sensory information from the periphery, but also act in communication with the motor cortex. To the best of our knowledge, this is the first study to empirically demonstrate that muscle fatigue leads to changes in interaction between structures of a brain’s neural network. In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant‐load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact‐free periods of 1‐min duration.
AbstractList In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant-load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact-free periods of 1-min duration. To quantify fatigue-induced intracortical communication, mean intra-hemispheric lagged phase synchronization between mid/anterior insular and motor cortex was calculated: (i) at the beginning of cycling; (ii) at the end of cycling; and (iii) during recovery cycling. Results revealed significantly increased lagged phase synchronization at the end of cycling, which returned to baseline during recovery cycling after subjects' cessation of exercise. Following previous imaging studies reporting the mid/anterior insular cortex as an essential instance processing a variety of sensory stimuli and signalling forthcoming physiological threat, our results provide further evidence that during a fatiguing exercise this structure might not only integrate and evaluate sensory information from the periphery, but also act in communication with the motor cortex. To the best of our knowledge, this is the first study to empirically demonstrate that muscle fatigue leads to changes in interaction between structures of a brain's neural network. In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant-load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact-free periods of 1-min duration.
In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant-load test at 60% peak oxygen consumption (VO(2peak)) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact-free periods of 1-min duration. To quantify fatigue-induced intracortical communication, mean intra-hemispheric lagged phase synchronization between mid/anterior insular and motor cortex was calculated: (i) at the beginning of cycling; (ii) at the end of cycling; and (iii) during recovery cycling. Results revealed significantly increased lagged phase synchronization at the end of cycling, which returned to baseline during recovery cycling after subjects' cessation of exercise. Following previous imaging studies reporting the mid/anterior insular cortex as an essential instance processing a variety of sensory stimuli and signalling forthcoming physiological threat, our results provide further evidence that during a fatiguing exercise this structure might not only integrate and evaluate sensory information from the periphery, but also act in communication with the motor cortex. To the best of our knowledge, this is the first study to empirically demonstrate that muscle fatigue leads to changes in interaction between structures of a brain's neural network.In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant-load test at 60% peak oxygen consumption (VO(2peak)) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact-free periods of 1-min duration. To quantify fatigue-induced intracortical communication, mean intra-hemispheric lagged phase synchronization between mid/anterior insular and motor cortex was calculated: (i) at the beginning of cycling; (ii) at the end of cycling; and (iii) during recovery cycling. Results revealed significantly increased lagged phase synchronization at the end of cycling, which returned to baseline during recovery cycling after subjects' cessation of exercise. Following previous imaging studies reporting the mid/anterior insular cortex as an essential instance processing a variety of sensory stimuli and signalling forthcoming physiological threat, our results provide further evidence that during a fatiguing exercise this structure might not only integrate and evaluate sensory information from the periphery, but also act in communication with the motor cortex. To the best of our knowledge, this is the first study to empirically demonstrate that muscle fatigue leads to changes in interaction between structures of a brain's neural network.
In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant‐load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact‐free periods of 1‐min duration. To quantify fatigue‐induced intracortical communication, mean intra‐hemispheric lagged phase synchronization between mid/anterior insular and motor cortex was calculated: (i) at the beginning of cycling; (ii) at the end of cycling; and (iii) during recovery cycling. Results revealed significantly increased lagged phase synchronization at the end of cycling, which returned to baseline during recovery cycling after subjects’ cessation of exercise. Following previous imaging studies reporting the mid/anterior insular cortex as an essential instance processing a variety of sensory stimuli and signalling forthcoming physiological threat, our results provide further evidence that during a fatiguing exercise this structure might not only integrate and evaluate sensory information from the periphery, but also act in communication with the motor cortex. To the best of our knowledge, this is the first study to empirically demonstrate that muscle fatigue leads to changes in interaction between structures of a brain’s neural network. In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant‐load test at 60% peak oxygen consumption (VO2peak) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact‐free periods of 1‐min duration.
In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16 healthy male subjects performing a constant-load test at 60% peak oxygen consumption (VO(2peak)) until volitional exhaustion, electroencephalography data were analysed during repetitive, artefact-free periods of 1-min duration. To quantify fatigue-induced intracortical communication, mean intra-hemispheric lagged phase synchronization between mid/anterior insular and motor cortex was calculated: (i) at the beginning of cycling; (ii) at the end of cycling; and (iii) during recovery cycling. Results revealed significantly increased lagged phase synchronization at the end of cycling, which returned to baseline during recovery cycling after subjects' cessation of exercise. Following previous imaging studies reporting the mid/anterior insular cortex as an essential instance processing a variety of sensory stimuli and signalling forthcoming physiological threat, our results provide further evidence that during a fatiguing exercise this structure might not only integrate and evaluate sensory information from the periphery, but also act in communication with the motor cortex. To the best of our knowledge, this is the first study to empirically demonstrate that muscle fatigue leads to changes in interaction between structures of a brain's neural network.
Author Lutz, Kai
Boutellier, Urs
Langer, Nicolas
Hilty, Lea
Pascual-Marqui, Roberto
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  surname: Hilty
  fullname: Hilty, Lea
  organization: Exercise Physiology, Institute of Human Movement Sciences, ETH Zurich, Zurich, Switzerland
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  givenname: Nicolas
  surname: Langer
  fullname: Langer, Nicolas
  organization: Institute of Psychology, Department of Neuropsychology, University of Zurich, Switzerland
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  fullname: Pascual-Marqui, Roberto
  organization: The KEY Institute for Brain-Mind Research, University Hospital of Psychiatry, Zurich, Switzerland
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  surname: Boutellier
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  organization: Exercise Physiology, Institute of Human Movement Sciences, ETH Zurich, Zurich, Switzerland
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  givenname: Kai
  surname: Lutz
  fullname: Lutz, Kai
  organization: Institute of Psychology, Department of Neuropsychology, University of Zurich, Switzerland
BackLink https://www.ncbi.nlm.nih.gov/pubmed/22097899$$D View this record in MEDLINE/PubMed
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Tajima, S., Yamamoto, S., Tanaka, M., Kataoka, Y., Iwase, M., Yoshikawa, E., Okada, H., Onoe, H., Tsukada, H., Kuratsune, H., Ouchi, Y. & Watanabe, Y. (2010) Medial orbitofrontal cortex is associated with fatigue sensation. Neurol. Res. Int., doi: 10.1155/2010/671421 [Epub ahead of print].
Pascual-Marqui, R.D., Lehmann, D., Koukkou, M., Kochi, K., Anderer, P., Saletu, B., Tanaka, H., Hirata, K., John, E.R., Prichep, L., Biscay-Lirio, R. & Kinoshita, T. (2011) Assessing interactions in the brain with exact low resolution electromagnetic tomography (eLORETA). Philos. Trans. R. Soc. Lond. A, 369, 3768-3784.
Reiman, E.M. (1997) The application of positron emission tomography to the study of normal and pathologic emotions. J. Clin. Psychiatry, 58(Suppl 16), 4-12.
Pascual-Marqui, R.D. (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find. Exp. Clin. Pharmacol., 24(Suppl D), 5-12.
Pfurtscheller, G., Brunner, C., Schlogl, A. & Lopes da Silva, F.H. (2006) Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks. Neuroimage, 31, 153-159.
Taylor, J.L., Butler, J.E., Allen, G.M. & Gandevia, S.C. (1996) Changes in motor cortical excitability during human muscle fatigue. J. Physiol., 490, 519-528.
Craig, A.D. (2003a) Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol., 13, 500-505.
Stam, C.J., Nolte, G. & Daffertshofer, A. (2007) Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Hum. Brain Mapp., 28, 1178-1193.
Binkofski, F., Schnitzler, A., Enck, P., Frieling, T., Posse, S., Seitz, R.J. & Freund, H.J. (1998) Somatic and limbic cortex activation in esophageal distention: a functional magnetic resonance imaging study. Ann. Neurol., 44, 811-815.
Craig, A.D., Chen, K., Bandy, D. & Reiman, E.M. (2000) Thermosensory activation of insular cortex. Nat. Neurosci., 3, 184-190.
Cannon, W.B. (1935) Stresses and strains of homeostasis. Am. J. Med. Sci., 189, 13-14.
Picard, N. & Strick, P.L. (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex, 6, 342-353.
Hilty, L., Lutz, K., Maurer, K., Rodenkirch, T., Spengler, C.M., Boutellier, U., Jancke, L. & Amann, M. (2011) Spinal opioid receptor-sensitive muscle afferents contribute to the fatigue-induced increase in intracortical inhibition in healthy humans. Exp. Physiol., 96, 505-517.
Craig, A.D., Bushnell, M.C., Zhang, E.T. & Blomqvist, A. (1994) A thalamic nucleus specific for pain and temperature sensation. Nature, 372, 770-773.
Noakes, T.D., St Clair Gibson, A. & Lambert, E.V. (2005) From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans: summary and conclusions. Br. J. Sports Med., 39, 120-124.
Florian, G., Andrew, C. & Pfurtscheller, G. (1998) Do changes in coherence always reflect changes in functional coupling? Electroencephalogr. Clin. Neurophysiol., 106, 87-91.
Casey, K.L. (1999) Forebrain mechanisms of nociception and pain: analysis through imaging. Proc. Natl. Acad. Sci. USA, 96, 7668-7674.
Hilty, L., Jancke, L., Luechinger, R., Boutellier, U. & Lutz, K. (2010) Limitation of physical performance in a muscle fatiguing handgrip exercise is mediated by thalamo-insular activity. Hum. Brain Mapp., doi: 10.1002/hbm.21177 [Epub ahead of print].
Craig, A.D. (2003b) A new view of pain as a homeostatic emotion. Trends Neurosci., 26, 303-307.
Fuchs, M., Kastner, J., Wagner, M., Hawes, S. & Ebersole, J.S. (2002) A standardized boundary element method volume conductor model. Clin. Neurophysiol., 113, 702-712.
McClure, S.M., Laibson, D.I., Loewenstein, G. & Cohen, J.D. (2004) Separate neural systems value immediate and delayed monetary rewards. Science, 306, 503-507.
Liu, J.Z., Dai, T.H., Sahgal, V., Brown, R.W. & Yue, G.H. (2002) Nonlinear cortical modulation of muscle fatigue: a functional MRI study. Brain Res., 957, 320-329.
Nybo, L. & Nielsen, B. (2001) Perceived exertion is associated with an altered brain activity during exercise with progressive hyperthermia. J. Appl. Physiol., 91, 2017-2023.
Pfurtscheller, G., Neuper, C. & Krausz, G. (2000) Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement. Clin. Neurophysiol., 111, 1873-1879.
Schneider, S., Brummer, V., Abel, T., Askew, C.D. & Struder, H.K. (2009) Changes in brain cortical activity measured by EEG are related to individual exercise preferences. Physiol. Behav., 98, 447-452.
Fitts, R.H. & Holloszy, J.O. (1976) Lactate and contractile force in frog muscle during development of fatigue and recovery. Am. J. Physiol., 231, 430-433.
Laibson, D. (1997) Golden eggs and hyperbolic discounting. Quart. J. Econ., 112, 443-478.
Brannan, S., Liotti, M., Egan, G., Shade, R., Madden, L., Robillard, R., Abplanalp, B., Stofer, K., Denton, D. & Fox, P.T. (2001) Neuroimaging of cerebral activations and deactivations associated with hypercapnia and hunger for air. Proc. Natl. Acad. Sci. USA, 98, 2029-2034.
Liu, J.Z., Shan, Z.Y., Zhang, L.D., Sahgal, V., Brown, R.W. & Yue, G.H. (2003) Human brain activation during sustained and intermittent submaximal fatigue muscle contractions: an FMRI study. J. Neurophysiol., 90, 300-312.
Taylor, J.L., Petersen, N., Butler, J.E. & Gandevia, S.C. (2000) Ischaemia after exercise does not reduce responses of human motoneurones to cortical or corticospinal tract stimulation. J. Physiol., 525, 793-801.
Laufs, H., Kleinschmidt, A., Beyerle, A., Eger, E., Salek-Haddadi, A., Preibisch, C. & Krakow, K. (2003) EEG-correlated fMRI of human alpha activity. Neuroimage, 19, 1463-1476.
Porter, L.L. & Sakamoto, K. (1988) Organization and synaptic relationships of the projection from the primary sensory to the primary motor cortex in the cat. J. Comp. Neurol., 271, 387-396.
Davidson, R.J. (1988) EEG measures of cerebral asymmetry: conceptual and methodological issues. Int. J. Neurosci., 39, 71-89.
Nolte, G., Bai, O., Wheaton, L., Mari, Z., Vorbach, S. & Hallett, M. (2004) Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin. Neurophysiol., 115, 2292-2307.
Baciu, M.V., Bonaz, B.L., Papillon, E., Bost, R.A., Le Bas, J.F., Fournet, J. & Segebarth, C.M. (1999) Central processing of rectal pain: a functional MR imaging study. Am. J. Neuroradiol., 20, 1920-1924.
Seymour, B., O'Doherty, J.P., Koltzenburg, M., Wiech, K., Frackowiak, R., Friston, K. & Dolan, R. (2005) Opponent appetitive-aversive neural processes underlie predictive learning of pain relief. Nat. Neurosci., 8, 1234-1240.
Gandevia, S.C., Allen, G.M., Butler, J.E. & Taylor, J.L. (1996) Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J. Physiol., 490, 529-536.
Liotti, M., Brannan, S., Egan, G., Shade, R., Madden, L., Abplanalp, B., Robillard, R., Lancaster, J., Zamarripa, F.E., Fox, P.T. & Denton, D. (2001) Brain responses associated with consciousness of breathlessness (air hunger). Proc. Natl. Acad. Sci. USA, 98, 2035-2040.
Kupers, R.C., Svensson, P. & Jensen, T.S. (2004) Central representation of muscle pain and mechanical hyperesthesia in the orofacial region: a positron emission tomography study. Pain, 108, 284-293.
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. J. Physiol., 586, 1277-1289.
St Clair Gibson, A. & Noakes, T.D. (2004) Evidence for complex system integration and dynamic neural regulation of skeletal muscle recruitment during exercise in humans. Br. J. Sports Med., 38, 797-806.
Nielsen, B., Hyldig, T., Bidstrup, F., Gonzalez-Alonso, J. & Christoffersen, G.R. (2001) Brain activity and fatigue during prolonged exercise in the heat. Pflugers Arch., 442, 41-48.
O'Donnell, R.D., Berkhout, J. & Adey, W.R. (1974) Contamination of scalp EEG spectrum during contraction of cranio-facial muscles. Electroencephalogr. Clin. Neurophysiol., 37, 145-151.
Schreurs, K.M., de Ridder, D.T. & Bensing, J.M. (2002) Fatigue in multiple sclerosis: reciprocal relationships with physical disabilities and depression. J. Psychosom. Res., 53, 775-781.
Kohler, G. & Boutellier, U. (2005) The generalized force-velocity relationship explains why the preferred pedaling rate of cyclists exceeds the most efficient one. Eur. J. Appl. Physiol., 94, 188-195.
Tataranni, P.A., Gautier, J.F., Chen, K., Uecker, A., Bandy, D., Salbe, A.D., Pratley, R.E., Lawson, M., Reiman,
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– volume: 113
  start-page: 702
  year: 2002
  end-page: 712
  article-title: A standardized boundary element method volume conductor model
  publication-title: Clin. Neurophysiol.
– volume: 91
  start-page: 2017
  year: 2001
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Snippet In the present study, intracortical communication between mid/anterior insular and motor cortex was investigated during a fatiguing cycling exercise. From 16...
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StartPage 2035
SubjectTerms Adult
Cerebral Cortex - anatomy & histology
Cerebral Cortex - physiology
EEG
Electroencephalography
exercise
Exercise - physiology
homeostatic functions
Humans
lagged phase synchronization
Male
Motor Cortex - physiology
Muscle Fatigue - physiology
Nerve Net - anatomy & histology
Nerve Net - physiology
supraspinal fatigue
Young Adult
Title Fatigue-induced increase in intracortical communication between mid/anterior insular and motor cortex during cycling exercise
URI https://api.istex.fr/ark:/67375/WNG-LFHJ8ZJS-Z/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1460-9568.2011.07909.x
https://www.ncbi.nlm.nih.gov/pubmed/22097899
https://www.proquest.com/docview/911932218
https://www.proquest.com/docview/920789401
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