Recent studies have shown that muscle alterations cannot totally explain peripheral muscle weakness in COPD. Cerebral abnormalities in COPD are well documented but have never been implicated in muscle torque production. The purpose of this study was to assess the neural correlates of quadriceps torque control in COPD patients. Fifteen patients (FEV1 54.1±3.6% predicted) and 15 age- and sex-matched healthy controls performed maximal (MVCs) and submaximal (SVCs) voluntary contractions at 10, 30 and 50% of the maximal voluntary torque of the knee extensors. Neural activity was quantified with changes in functional near-infrared spectroscopy oxyhemoglobin (fNIRS-HbO) over the contralateral primary motor (M1), primary somatosensory (S1), premotor (PMC) and prefrontal (PFC) cortical areas. In parallel to the lower muscle torque, the COPD patients showed lower increase in HbO than healthy controls over the M1 (p<0.05), PMC (p<0.05) and PFC areas (p<0.01) during MVCs. In addition, they exhibited lower HbO changes over the M1 (p<0.01), S1 (p<0.05) and PMC (p<0.01) areas during SVCs at 50% of maximal torque and altered motor control characterized by higher torque fluctuations around the target. The results show that low muscle force production is found in a context of reduced motor cortex activity, which is consistent with central nervous system involvement in COPD muscle weakness.
References
[1]
Gosselink R, Troosters T, Decramer M (1996) Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med 153: 976–980. doi: 10.1164/ajrccm.153.3.8630582
[2]
Decramer M, Gosselink R, Troosters T, Verschueren M, Evers G (1997) Muscle weakness is related to utilization of health care resources in COPD patients. Eur Respir J 10: 417–423. doi: 10.1183/09031936.97.10020417
[3]
Swallow EB, Reyes D, Hopkinson NS, Man WD, Porcher R, et al. (2007) Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease. Thorax 62: 115–120. doi: 10.1136/thx.2006.062026
[4]
Bernard S, LeBlanc P, Whittom F, Carrier G, Jobin J, et al. (1998) Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 158: 629–634. doi: 10.1164/ajrccm.158.2.9711023
[5]
Menon MK, Houchen L, Harrison S, Singh SJ, Morgan MD, et al. (2012) Ultrasound assessment of lower limb muscle mass in response to resistance training in COPD. Respir Res 13: 119. doi: 10.1186/1465-9921-13-119
[6]
Shrikrishna D, Patel M, Tanner RJ, Seymour JM, Connolly BA, et al. (2012) Quadriceps wasting and physical inactivity in patients with COPD. Eur Respir J 40: 1115–1122. doi: 10.1183/09031936.00170111
[7]
Clark BC, Manini TM (2008) Sarcopenia = / = dynapenia. J Gerontol A Biol Sci Med Sci 63: 829–834. doi: 10.1093/gerona/63.8.829
[8]
Lahousse L, Vernooij MW, Darweesh SK, Akoudad S, Loth DW, et al. (2013) Chronic obstructive pulmonary disease and cerebral microbleeds. The Rotterdam Study. Am J Respir Crit Care Med 188: 783–788. doi: 10.1164/rccm.201303-0455oc
[9]
Zhang H, Wang X, Lin J, Sun Y, Huang Y, et al. (2013) Reduced regional gray matter volume in patients with chronic obstructive pulmonary disease: a voxel-based morphometry study. AJNR Am J Neuroradiol 34: 334–339. doi: 10.3174/ajnr.a3235
[10]
Dodd JW, Chung AW, van den Broek MD, Barrick TR, Charlton RA, et al. (2012) Brain structure and function in chronic obstructive pulmonary disease: a multimodal cranial magnetic resonance imaging study. Am J Respir Crit Care Med 186: 240–245. doi: 10.1164/rccm.201202-0355oc
[11]
Shim TS, Lee JH, Kim SY, Lim TH, Kim SJ, et al. (2001) Cerebral metabolic abnormalities in COPD patients detected by localized proton magnetic resonance spectroscopy. Chest 120: 1506–1513. doi: 10.1378/chest.120.5.1506
[12]
Oncel C, Baser S, Cam M, Akdag B, Taspinar B, et al. (2010) Peripheral neuropathy in chronic obstructive pulmonary disease. COPD 7: 11–16. doi: 10.3109/15412550903499480
[13]
Kirkil G, Tug T, Ozel E, Bulut S, Tekatas A, et al. (2007) The evaluation of cognitive functions with P300 test for chronic obstructive pulmonary disease patients in attack and stable period. Clin Neurol Neurosurg 109: 553–560. doi: 10.1016/j.clineuro.2007.03.013
[14]
Hopkinson NS, Sharshar T, Ross ET, Nickol AH, Dayer MJ, et al. (2004) Corticospinal control of respiratory muscles in chronic obstructive pulmonary disease. Respir Physiol Neurobiol 141: 1–12. doi: 10.1016/j.resp.2004.04.003
[15]
Mador MJ, Deniz O, Aggarwal A, Kufel TJ (2003) Quadriceps fatigability after single muscle exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 168: 102–108. doi: 10.1164/rccm.200202-080oc
[16]
Seymour JM, Ward K, Raffique A, Steier JS, Sidhu PS, et al. (2012) Quadriceps and ankle dorsiflexor strength in chronic obstructive pulmonary disease. Muscle Nerve 46: 548–554. doi: 10.1002/mus.23353
[17]
Vivodtzev I, Flore P, Levy P, Wuyam B (2008) Voluntary activation during knee extensions in severely deconditioned patients with chronic obstructive pulmonary disease: benefit of endurance training. Muscle Nerve 37: 27–35. doi: 10.1002/mus.20867
[18]
Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82: 2271–2283.
[19]
van Duinen H, Renken R, Maurits NM, Zijdewind I (2008) Relation between muscle and brain activity during isometric contractions of the first dorsal interosseus muscle. Hum Brain Mapp 29: 281–299. doi: 10.1002/hbm.20388
[20]
Derosiere G, Perrey S (2012) Relationship between submaximal handgrip muscle force and NIRS-measured motor cortical activation. Adv Exp Med Biol 737: 269–274. doi: 10.1007/978-1-4614-1566-4_40
[21]
Strangman G, Culver JP, Thompson JH, Boas DA (2002) A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17: 719–731. doi: 10.1006/nimg.2002.1227
[22]
Sato H, Yahata N, Funane T, Takizawa R, Katura T, et al. (2013) A NIRS-fMRI investigation of prefrontal cortex activity during a working memory task. Neuroimage 83: 158–173. doi: 10.1016/j.neuroimage.2013.06.043
[23]
Mehagnoul-Schipper DJ, van der Kallen BF, Colier WN, van der Sluijs MC, van Erning LJ, et al. (2002) Simultaneous measurements of cerebral oxygenation changes during brain activation by near-infrared spectroscopy and functional magnetic resonance imaging in healthy young and elderly subjects. Hum Brain Mapp 16: 14–23. doi: 10.1002/hbm.10026
[24]
Higashimoto Y, Honda N, Yamagata T, Matsuoka T, Maeda K, et al. (2011) Activation of the prefrontal cortex is associated with exertional dyspnea in chronic obstructive pulmonary disease. Respiration 82: 492–500. doi: 10.1159/000324571
[25]
Lin PY, Chen JJ, Lin SI (2013) The cortical control of cycling exercise in stroke patients: an fNIRS study. Hum Brain Mapp 34: 2381–2390. doi: 10.1002/hbm.22072
[26]
Mehta RK, Shortz AE (2013) Obesity-related differences in neural correlates of force control. Eur J Appl Physiol.
[27]
Perrey S (2008) Non-invasive NIR spectroscopy of human brain function during exercise. Methods 45: 289–299. doi: 10.1016/j.ymeth.2008.04.005
[28]
Ekkekakis P (2009) Illuminating the black box: investigating prefrontal cortical hemodynamics during exercise with near-infrared spectroscopy. J Sport Exerc Psychol 31: 505–553.
[29]
Fox PT, Raichle ME, Mintun MA, Dence C (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science 241: 462–464. doi: 10.1126/science.3260686
[30]
Colier WN, Quaresima V, Oeseburg B, Ferrari M (1999) Human motor-cortex oxygenation changes induced by cyclic coupled movements of hand and foot. Exp Brain Res 129: 457–461. doi: 10.1007/s002210050913
[31]
Guideline thirteen: guidelines for standard electrode position nomenclature. American Electroencephalographic Society. J Clin Neurophysiol 11: 111–113. doi: 10.1097/00004691-199401000-00014
[32]
Duncan A, Meek JH, Clemence M, Elwell CE, Fallon P, et al. (1996) Measurement of cranial optical path length as a function of age using phase resolved near infrared spectroscopy. Pediatr Res 39: 889–894. doi: 10.1203/00006450-199605000-00025
[33]
Chow JW, Stokic DS (2011) Force control of quadriceps muscle is bilaterally impaired in subacute stroke. J Appl Physiol (1985) 111: 1290–1295. doi: 10.1152/japplphysiol.00462.2011
[34]
Missenard O, Mottet D, Perrey S (2008) Muscular fatigue increases signal-dependent noise during isometric force production. Neurosci Lett 437: 154–157. doi: 10.1016/j.neulet.2008.03.090
[35]
Minagawa-Kawai Y, van der Lely H, Ramus F, Sato Y, Mazuka R, et al. (2011) Optical brain imaging reveals general auditory and language-specific processing in early infant development. Cereb Cortex 21: 254–261. doi: 10.1093/cercor/bhq082
[36]
Voorrips LE, Ravelli AC, Dongelmans PC, Deurenberg P, Van Staveren WA (1991) A physical activity questionnaire for the elderly. Med Sci Sports Exerc 23: 974–979. doi: 10.1249/00005768-199108000-00015
[37]
Mador MJ, Bozkanat E (2001) Skeletal muscle dysfunction in chronic obstructive pulmonary disease. Respir Res 2: 216–224. doi: 10.1186/rr60
[38]
Yildiz S, Kaya I, Cece H, Gencer M, Ziylan Z, et al. (2012) Impact of COPD exacerbation on cerebral blood flow. Clin Imaging 36: 185–190. doi: 10.1016/j.clinimag.2011.08.021
[39]
Albayrak R, Fidan F, Unlu M, Sezer M, Degirmenci B, et al. (2006) Extracranial carotid Doppler ultrasound evaluation of cerebral blood flow volume in COPD patients. Respir Med 100: 1826–1833. doi: 10.1016/j.rmed.2006.01.015
[40]
Nishimura Y, Onoe H, Morichika Y, Tsukada H, Isa T (2007) Activation of parieto-frontal stream during reaching and grasping studied by positron emission tomography in monkeys. Neurosci Res 59: 243–250. doi: 10.1016/j.neures.2007.07.003
[41]
Manto M, Bower JM, Conforto AB, Delgado-Garcia JM, da Guarda SN, et al. (2012) Consensus paper: roles of the cerebellum in motor control–the diversity of ideas on cerebellar involvement in movement. Cerebellum 11: 457–487. doi: 10.1007/s12311-011-0331-9
[42]
Paulin MG (1993) The role of the cerebellum in motor control and perception. Brain Behav Evol 41: 39–50. doi: 10.1159/000113822
[43]
Dodd JW, Getov SV, Jones PW (2010) Cognitive function in COPD. Eur Respir J 35: 913–922. doi: 10.1183/09031936.00125109
[44]
Kramer AF, Erickson KI (2007) Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends Cogn Sci 11: 342–348. doi: 10.1016/j.tics.2007.06.009
