Human brain activation during sustained and intermittent submaximal fatigue muscle contractions: an FMRI study.

During prolonged submaximal muscle contractions, electromyographic (EMG) signals typically increase as a result of increasing motor unit activities to compensate for fatigue-induced force loss in the muscle. It is thought that cortical signals driving the muscle to higher activation levels also increases, but this has never been experimentally demonstrated. The purpose of this study was to quantify brain activation during submaximal fatigue muscle contractions using functional magnetic resonance imaging (fMRI). Twelve volunteers performed a sustained handgrip contraction for 225 s and 320 intermittent handgrip contractions ( approximately 960 s) at 30% maximal level while their brain was imaged. For the sustained contraction, EMG signals of the finger flexor muscles increased linearly while the target force was maintained. The fMRI-measured cortical activities in the contralateral sensorimotor cortex increased sharply during the first 150 s, then plateaued during the last 75 s. For the intermittent contractions, the EMG signals increased during the first 660 s and then began to decline, while the handgrip force also showed a sign of decrease despite maximal effort to maintain the force. The fMRI signal of the contralateral sensorimotor area showed a linear rise for most part of the task and plateaued at the end. For both the tasks, the fMRI signals in the ipsilateral sensorimotor cortex, prefrontal cortex, cingulate gyrus, supplementary motor area, and cerebellum exhibited steady increases. These results showed that the brain increased its output to reinforce the muscle for the continuation of the performance and possibly to process additional sensory information.

[1]  M. Johnson,et al.  Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. , 1973, Journal of the neurological sciences.

[2]  Volker Dietz,et al.  Analysis of the electrical muscle activity during maximal contraction and the influence of ischaemia , 1978, Journal of the Neurological Sciences.

[3]  Allan M. Smith The activity of supplementary motor area neurons during a maintained precision grip , 1979, Brain Research.

[4]  A. M. Smith The coactivation of antagonist muscles. , 1981, Canadian journal of physiology and pharmacology.

[5]  B Bigland-Ritchie,et al.  EMG/FORCE RELATIONS AND FATIGUE OF HUMAN VOLUNTARY CONTRACTIONS , 1981, Exercise and sport sciences reviews.

[6]  R. Johansson,et al.  Changes in motoneurone firing rates during sustained maximal voluntary contractions. , 1983, The Journal of physiology.

[7]  B. Bigland-ritchie,et al.  Fatigue of intermittent submaximal voluntary contractions: central and peripheral factors. , 1986, Journal of applied physiology.

[8]  G. A. Young,et al.  The bootstrap: To smooth or not to smooth? , 1987 .

[9]  W. Z. Rymer,et al.  Increased inhibitory effects on close synergists during muscle fatigue in the decerebrate cat , 1988, Brain Research.

[10]  S. Garner,et al.  Reduced voluntary electromyographic activity after fatiguing stimulation of human muscle. , 1988, The Journal of physiology.

[11]  W. Rymer,et al.  Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae. , 1991, Journal of neurophysiology.

[12]  S. Garland,et al.  Role of small diameter afferents in reflex inhibition during human muscle fatigue. , 1991, The Journal of physiology.

[13]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D G Stuart,et al.  Neurobiology of muscle fatigue. , 1992, Journal of applied physiology.

[15]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[16]  Mitsumasa Iwamoto,et al.  Generation of Maxwell displacement current from spread monolayers containing azobenzene , 1992 .

[17]  A J Fuglevand,et al.  Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. , 1993, The Journal of physiology.

[18]  Ravi S. Menon,et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. , 1993, Biophysical journal.

[19]  E Cafarelli,et al.  Behavior of coactive muscles during fatigue. , 1993, Journal of applied physiology.

[20]  Ravi S. Menon,et al.  Functional imaging of human motor cortex at high magnetic field. , 1993, Journal of neurophysiology.

[21]  W. Darling,et al.  Variations in soleus H-reflexes as a function of plantarflexion torque in man , 1993, Brain Research.

[22]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[23]  Jean-Baptiste Poline,et al.  Analysis of individual brain activation maps using hierarchical description and multiscale detection , 1994, IEEE Trans. Medical Imaging.

[24]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[25]  G. A. Robinson,et al.  Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. , 1994, Journal of applied physiology.

[26]  M. Bushnell,et al.  A thalamic nucleus specific for pain and temperature sensation , 1994, Nature.

[27]  M Hallett,et al.  Central fatigue as revealed by postexercise decrement of motor evoked potentials , 1994, Muscle & nerve.

[28]  J B Poline,et al.  Enhanced Detection in Brain Activation Maps Using a Multifiltering Approach , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  D. Siegmund,et al.  Testing for a Signal with Unknown Location and Scale in a Stationary Gaussian Random Field , 1995 .

[30]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[31]  A J Fuglevand,et al.  The role of the sarcolemma action potential in fatigue. , 1995, Advances in experimental medicine and biology.

[32]  Simon C. Gandevia,et al.  Fatigue : neural and muscular mechanisms , 1995 .

[33]  S. Gandevia,et al.  Fatigue brought on by malfunction of the central and peripheral nervous systems. , 1995, Advances in experimental medicine and biology.

[34]  R. Enoka,et al.  Short-term immobilization has a minimal effect on the strength and fatigability of a human hand muscle. , 1995, Journal of applied physiology.

[35]  S. Garland,et al.  Role of muscle afferents in the inhibition of motoneurons during fatigue. , 1995, Advances in experimental medicine and biology.

[36]  A. Kimura,et al.  Motor unit firing behavior in slow and fast contractions of the first dorsal interosseous muscle of healthy men. , 1995, Electroencephalography and clinical neurophysiology.

[37]  D. Wolf,et al.  Molecular‐dynamics study of the synthesis and characterization of a fully dense, three‐dimensional nanocrystalline material , 1995 .

[38]  K. Worsley Estimating the number of peaks in a random field using the Hadwiger characteristic of excursion sets, with applications to medical images , 1995 .

[39]  Richard S. J. Frackowiak,et al.  Cerebral activation during the exertion of sustained static force in man , 1996, Neuroreport.

[40]  Stephan Arndt,et al.  Normalizing Counts and Cerebral Blood Flow Intensity in Functional Imaging Studies of the Human Brain , 1996, NeuroImage.

[41]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[42]  J. L. Taylor,et al.  Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. , 1996, The Journal of physiology.

[43]  M. Bilodeau,et al.  Task‐dependent effect of limb immobilization on the fatigability of the elbow flexor muscles in humans , 1997, Experimental physiology.

[44]  David G. Behm,et al.  Effects of fatigue duration and muscle type on voluntary and evoked contractile properties. , 1997, Journal of applied physiology.

[45]  A. Kossev,et al.  Motor unit activity during long-lasting intermittent muscle contractions in humans , 1998, European Journal of Applied Physiology and Occupational Physiology.

[46]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[47]  A. Fuglevand,et al.  Cessation of human motor unit discharge during sustained maximal voluntary contraction , 1999, Neuroscience Letters.

[48]  S C Gandevia,et al.  Supraspinal fatigue during intermittent maximal voluntary contractions of the human elbow flexors. , 2000, Journal of applied physiology.

[49]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[50]  Jing Z. Liu,et al.  Simultaneous measurement of human joint force, surface electromyograms, and functional MRI-measured brain activation , 2000, Journal of Neuroscience Methods.

[51]  D. G. Albrecht,et al.  Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? , 2000, Nature Neuroscience.

[52]  Mark Woolrich,et al.  Lowpass temporal filtering in FMRI time series , 2000, NeuroImage.

[53]  Guang H. Yue,et al.  Relationship between motor activity-related cortical potential and voluntary muscle activation , 2000, Experimental Brain Research.

[54]  Dae-Shik Kim,et al.  Spatiotemporal dynamics of the BOLD fMRI signals: Toward mapping submillimeter cortical columns using the early negative response , 2000, Magnetic resonance in medicine.

[55]  Karl J. Friston,et al.  To Smooth or Not to Smooth? Bias and Efficiency in fMRI Time-Series Analysis , 2000, NeuroImage.

[56]  Jing Z. Liu,et al.  Brain activation during human finger extension and flexion movements , 2000, Brain Research.

[57]  J. Duchateau,et al.  Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus , 2001, The Journal of physiology.

[58]  Jing Z. Liu,et al.  Relationship between muscle output and functional MRI-measured brain activation , 2001, Experimental Brain Research.

[59]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[60]  S. Gandevia Spinal and supraspinal factors in human muscle fatigue. , 2001, Physiological reviews.

[61]  Marcus E. Raichle,et al.  Cognitive neuroscience: Bold insights , 2001, Nature.

[62]  Jing Z. Liu,et al.  Nonlinear cortical modulation of muscle fatigue: a functional MRI study , 2002, Brain Research.

[63]  The Muscular Wisdom Hypothesis in Human Muscle Fatigue , 2002, Exercise and sport sciences reviews.

[64]  Garland Sj,et al.  The muscular wisdom hypothesis in human muscle fatigue. , 2002 .

[65]  A. Thorstensson,et al.  Central fatigue during a long-lasting submaximal contraction of the triceps surae , 1996, Experimental Brain Research.