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Changes of cortico-muscular coherence: an early marker of healthy aging?

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Abstract

Cortico-muscular coherence (CMC) at beta frequency (13–30 Hz) occurs particularly during weak to moderate isometric contraction. It is a well-established measure of communication between the primary motor cortex (M1) and corresponding muscles revealing information about the integrity of the pyramidal system. Although the slowing of brain and muscle dynamics during healthy aging has been evidenced, functional communication as determined by CMC has not been investigated so far. Since decline of motor functions at higher age is likely to be associated with CMC changes, the present study aims at shedding light on the functionality of the motor system from a functional interaction perspective. To this end, CMC was investigated in 27 healthy subjects aging between 22 and 77 years during isometric contraction of their right forearm. Neuromagnetic activity was measured using whole-head magnetoencephalography (MEG). Muscle activity was measured by means of surface electromyography (EMG) of the right extensor digitorum communis (EDC) muscle. Additionally, MEG-EMG phase lags were calculated in order to estimate conducting time. The analysis revealed CMC and M1 power amplitudes to be increased with age accompanied by slowing of M1, EMG, and CMC. Frequency changes were particularly found in subjects aged above 40 years suggesting that at this middle age, neurophysiological changes occur, possibly reflecting an early neurophysiological marker of seniority. Since MEG–EMG phase lags did not vary with age, changes cannot be explained by alterations of nerve conduction. We argue that the M1 power amplitude increase and the shift towards lower frequencies might represent a neurophysiological marker of healthy aging which is possibly compensated by increased CMC amplitude.

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References

  • Ahonen AI, Hamalainen MS, Ilmoniemi RJ, Kajola MJ, Knuutila JE, Simola JT, Vilkman VA (1993) Sampling theory for neuromagnetic detector arrays. IEEE Trans Biomed Eng 40:859–869

    Article  PubMed  CAS  Google Scholar 

  • Andrykiewicz A, Patino L, Naranjo JR, Witte M, Hepp-Reymond MC, Kristeva R (2007) Corticomuscular synchronization with small and large dynamic force output. BMC Neurosci 8:101

    Article  PubMed  Google Scholar 

  • Babiloni C, Binetti G, Cassarino A, Dal Forno G, Del Percio C, Ferreri F, Ferri R, Frisoni G, Galderisi S, Hirata K, Lanuzza B, Miniussi C, Mucci A, Nobili F, Rodriguez G, Luca Romani G, Rossini PM (2006) Sources of cortical rhythms in adults during physiological aging: a multicentric EEG study. Hum Brain Mapp 27:162–172

    Article  PubMed  Google Scholar 

  • Baker MR, Baker SN (2003) The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man. J Physiol 546:931–942

    Article  PubMed  CAS  Google Scholar 

  • Boonstra TW, van Wijk BC, Praamstra P, Daffertshofer A (2009) Corticomuscular and bilateral EMG coherence reflect distinct aspects of neural synchronization. Neurosci Lett 463:17–21

    Article  PubMed  CAS  Google Scholar 

  • Brown P (2000) Cortical drives to human muscle: the Piper and related rhythms. Prog Neurobiol 60:97–108

    Article  PubMed  CAS  Google Scholar 

  • Brown WF, Strong MJ, Snow R (1988) Methods for estimating numbers of motor-units in biceps-brachialis muscles and losses of motor-units with aging. Muscle Nerve 11:423–432

    Article  PubMed  CAS  Google Scholar 

  • Chakarov V, Naranjo JR, Schulte-Monting J, Omlor W, Huethe F, Kristeva R (2009) Betarange EEG-EMG coherence with isometric compensation for increasing modulated low-level forces. J Neurophysiol 102:1115–1120

    Article  PubMed  Google Scholar 

  • Classen J, Gerloff C, Honda M, Hallett M (1998) Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. J Neurophysiol 79:1567–1573

    PubMed  CAS  Google Scholar 

  • Conway B, Halliday D, Farmer S, Shahani U, Maas P, Weir A, Rosenberg J (1995) Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task. J Physiol 489:917–924

    PubMed  CAS  Google Scholar 

  • Derambure P, Defebvre L, Dujardin K, Bourriez JL, Jacquesson JM, Destee A, Guieu JD (1993) Effect of aging on the spatio-temporal pattern of event-related desynchronization during a voluntary movement. Electroencephalogr Clin Neurophysiol 89:197–203

    Article  PubMed  CAS  Google Scholar 

  • D'Esposito M, Zarahn E, Aguirre GK, Rypma B (1999) The effect of normal aging on the coupling of neural activity to the bold hemodynamic response. Neuroimage 10:6–14

    Article  PubMed  Google Scholar 

  • Doherty TJ, Vandervoort AA, Taylor AW, Brown WF (1993) Effects of motor-unit losses on strength in older men and women. J Appl Physiol 74:868–874

    Article  PubMed  CAS  Google Scholar 

  • Erim Z, Beg MF, Burke DT, de Luca CJ (1999) Effects of aging on motor-unit control properties. J Neurophysiol 82:2081–2091

    PubMed  CAS  Google Scholar 

  • Esposito F, Malgrati D, Veicsteinas A, Orizio C (1996) Time and frequency domain analysis of electromyogram and sound myogram in the elderly. Eur J Appl Physiol Occup Physiol 73:503–510

    Article  PubMed  CAS  Google Scholar 

  • Gross J, Kujala J, Hamalainen M, Timmermann L, Schnitzler A, Salmelin R (2001) Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Natl Acad Sci USA 98:694–699

    Article  PubMed  CAS  Google Scholar 

  • Gross J, Tass PA, Salenius S, Hari R, Freund HJ, Schnitzler A (2000) Cortico-muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencephalography. J Physiol 527(Pt 3):623–631

    Article  PubMed  CAS  Google Scholar 

  • Halliday DM, Conway BA, Farmer SF, Rosenberg JR (1998) Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci Lett 241:5–8

    Article  PubMed  CAS  Google Scholar 

  • Hari R, Salmelin R (1997) Human cortical oscillations: a neuromagnetic view through the skull. TINS 20:44–49

    PubMed  CAS  Google Scholar 

  • Heuninckx S, Wenderoth N, Debaere F, Peeters R, Swinnen SP (2005) Neural basis of aging: the penetration of cognition into action control. J Neurosci 25:6787–6796

    Article  PubMed  CAS  Google Scholar 

  • James LM, Halliday DM, Stephens JA, Farmer SF (2008) On the development of human corticospinal oscillations: age-related changes in EEG-EMG coherence and cumulant. Eur J Neurosci 27:3369–3379

    Article  PubMed  Google Scholar 

  • Kilner JM, Baker SN, Salenius S, Hari R, Lemon RN (2000) Human cortical muscle coherence is directly related to specific motor parameters. J Neurosci 20:8838–8845

    PubMed  CAS  Google Scholar 

  • Kilner JM, Baker SN, Salenius S, Jousmaki V, Hari R, Lemon RN (1999) Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles. J Physiol 516(Pt 2):559–570

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Lee YS, Lee JJ, Song HJ, Yoo DS, Lee HJ, Kim HJ, Chang Y (2010) Functional magnetic resonance imaging reveals age-related alterations to motor networks in weighted elbow flexion-extension movement. Neurol Res 32:995–1001

    Article  PubMed  Google Scholar 

  • Krampe RT (2002) Aging, expertise and fine motor movement. Neurosci Biobehav Rev 26:769–776

    Article  PubMed  Google Scholar 

  • Kristeva R, Patino L, Omlor W (2007) Betarange cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output. Neuroimage 36:785–792

    Article  PubMed  Google Scholar 

  • Mackay WA (1997) Synchronized neuronal oscillations and their role in motor processes. Trends Cogn Sci 1:176–183

    Article  PubMed  CAS  Google Scholar 

  • Mima T, Hallett M (1999) Corticomuscular coherence: a review. J Clin Neurophysiol 16:501–511

    Article  PubMed  CAS  Google Scholar 

  • Mima T, Steger J, Schulman AE, Gerloff C, Hallett M (2000) Electroencephalographic measurement of motor cortex control of muscle activity in humans. Clin Neurophysiol 111:326–337

    Article  PubMed  CAS  Google Scholar 

  • Noble JW, Eng JJ, Kokotilo KJ, Boyd LA (2011) Aging effects on the control of grip force magnitude: an fMRI study. Exp Gerontol 46:453–461

    Article  PubMed  Google Scholar 

  • Olafsdottir H, Zhang W, Zatsiorsky VM, Latash ML (2007) Age-related changes in multifinger synergies in accurate moment of force production tasks. J Appl Physiol 102:1490–1501

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Omlor W, Patino L, Hepp-Reymond MC, Kristeva R (2007) Gammarange corticomuscular coherence during dynamic force output. Neuroimage 34:1191–1198

    Article  PubMed  Google Scholar 

  • Pfurtscheller G (1977) Graphical display and statistical evaluation of event-related desynchronization (ERD). Electroencephalogr Clin Neurophysiol 43:757–760

    Article  PubMed  CAS  Google Scholar 

  • Pfurtscheller G, Aranibar A (1977) Event-related cortical desynchronization detected by power measurements of scalp EEG. Electroencephalogr Clin Neurophysiol 42:817–826

    Article  PubMed  CAS  Google Scholar 

  • Pohja M, Salenius S, Hari R (2005) Reproducibility of cortex-muscle coherence. Neuroimage 26:764–770

    Article  PubMed  Google Scholar 

  • Raz N, Rodrigue KM (2006) Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev 30:730–748

    Article  PubMed  Google Scholar 

  • Riddle CN, Baker MR, Baker SN (2004) The effect of carbamazepine on human corticomuscular coherence. Neuroimage 22:333–340

    Article  PubMed  Google Scholar 

  • Sailer A, Dichgans J, Gerloff C (2000) The influence of normal aging on the cortical processing of a simple motor task. Neurology 55:979–985

    Article  PubMed  CAS  Google Scholar 

  • Salenius S, Hari R (2003) Synchronous cortical oscillatory activity during motor action. Curr Opin Neurobiol 13:678–684

    Article  PubMed  CAS  Google Scholar 

  • Salenius S, Portin K, Kajola M, Salmelin R, Hari R (1997) Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol 77:3401–3405

    PubMed  CAS  Google Scholar 

  • Schnitzler A, Gross J (2005) Normal and pathological oscillatory communication in the brain. Nat Neurosci Rev 6:285–296

    Article  CAS  Google Scholar 

  • Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34:721–733

    Article  PubMed  CAS  Google Scholar 

  • Semmler JG, Kornatz KW, Enoka RM (2003) Motor-unit coherence during isometric contractions is greater in a hand muscle of older adults. J Neurophysiol 90:1346–1349

    Article  PubMed  Google Scholar 

  • Wang FC, de Pasqua V, Delwaide PJ (1999) Age-related changes in fastest and slowest conducting axons of thenar motor-units. Muscle Nerve 22:1022–1029

    Article  PubMed  CAS  Google Scholar 

  • Ward NS (2006) Compensatory mechanisms in the aging motor system. Ageing Res Rev 5:239–254

    Article  PubMed  Google Scholar 

  • Ward NS, Frackowiak RS (2003) Age-related changes in the neural correlates of motor performance. Brain 126:873–888

    Article  PubMed  CAS  Google Scholar 

  • Witte M, Patino L, Andrykiewicz A, Hepp-Reymond MC, Kristeva R (2007) Modulation of human corticomuscular betarange coherence with low-level static forces. Eur J Neurosci 26:3564–3570

    Article  PubMed  Google Scholar 

  • Yang Q, Fang Y, Sun CK, Siemionow V, Ranganathan VK, Khoshknabi D, Davis MP, Walsh D, Sahgal V, Yue GH (2009) Weakening of functional corticomuscular coupling during muscle fatigue. Brain Res 1250:101–112

    Article  PubMed  CAS  Google Scholar 

  • Ziegler DA, Pritchett DL, Hosseini-Varnamkhasti P, Corkin S, Hamalainen M, Moore CI, Jones SR (2010) Transformations in oscillatory activity and evoked responses in primary somatosensory cortex in middle age: a combined computational neural modeling and MEG study. Neuroimage 52:897–912

    Article  PubMed  Google Scholar 

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Acknowledgments

Bettina Pollok is grateful for support from the Deutsche Forschungsgemeinschaft (PO 806/3-1) and from the Research Commission of the Medical Faculty of the Heinrich-Heine University (9772440). Vanessa Krause is grateful for financial support by a grant from Heinrich-Heine-University (9772467). We would like to thank Erika Rädisch for her technical support during MRI scans.

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Authors and Affiliations

  1. Institute of Clinical Neuroscience and Medical Psychology, Medical Faculty, University Düsseldorf, 40225, Düsseldorf, Germany

    Daniel Kamp, Vanessa Krause, Markus Butz, Alfons Schnitzler & Bettina Pollok

  2. Department of Neurology, Medical Faculty, University Düsseldorf, 40225, Düsseldorf, Germany

    Daniel Kamp, Vanessa Krause, Markus Butz, Alfons Schnitzler & Bettina Pollok

  3. Institute of Clinical Neuroscience and Medical Psychology, Medical Faculty, University Düsseldorf, Universitätsstr. 1, 40225, Düsseldorf, Germany

    Bettina Pollok

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  1. Daniel Kamp
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  2. Vanessa Krause
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  4. Alfons Schnitzler
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Correspondence to Bettina Pollok.

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Kamp, D., Krause, V., Butz, M. et al. Changes of cortico-muscular coherence: an early marker of healthy aging?. AGE 35, 49–58 (2013). https://doi.org/10.1007/s11357-011-9329-y

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  • DOI: https://doi.org/10.1007/s11357-011-9329-y

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