Low-Frequency Oscillations and Control of the Motor Output

A less precise force output impairs our ability to perform movements, learn new motor tasks, and use tools. Here we show that low-frequency oscillations in force are detrimental to force precision. We summarize the recent evidence that low-frequency oscillations in force output represent oscillations of the spinal motor neuron pool from the voluntary drive, and can be modulated by shifting power to higher frequencies. Further, force oscillations below 0.5 Hz impair force precision with increased voluntary drive, aging, and neurological disease. We argue that the low-frequency oscillations are (1) embedded in the descending drive as shown by the activation of multiple spinal motor neurons, (2) are altered with force intensity and brain pathology, and (3) can be modulated by visual feedback and motor training to enhance force precision. Thus, low-frequency oscillations in force provide insight into how the human brain regulates force precision.

[1]  B. Conway,et al.  Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. , 1995, The Journal of physiology.

[2]  Fan Wang,et al.  How the brainstem controls orofacial behaviors comprised of rhythmic actions , 2014, Trends in Neurosciences.

[3]  K M Newell,et al.  Variability and Noise in Continuous Force Production , 2000, Journal of motor behavior.

[4]  E. Christou,et al.  The interaction of respiration and visual feedback on the control of force and neural activation of the agonist muscle. , 2011, Human movement science.

[5]  Karl M Newell,et al.  Aging and the time and frequency structure of force output variability. , 2003, Journal of applied physiology.

[6]  Neha Lodha,et al.  Force Control Is Related to Low-Frequency Oscillations in Force and Surface EMG , 2014, PloS one.

[7]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[8]  G. Knyazev Motivation, emotion, and their inhibitory control mirrored in brain oscillations , 2007, Neuroscience & Biobehavioral Reviews.

[9]  D. Vaillancourt,et al.  Modulation of Force below 1 Hz: Age-Associated Differences and the Effect of Magnified Visual Feedback , 2013, PloS one.

[10]  Karl M Newell,et al.  The adaptive range of 1/f isometric force production. , 2009, Journal of experimental psychology. Human perception and performance.

[11]  E. M. Pinches,et al.  The role of synchrony and oscillations in the motor output , 1999, Experimental Brain Research.

[12]  R. Enoka,et al.  Mechanisms that contribute to differences in motor performance between young and old adults. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[13]  Carlo J. Deluc CONTROL PROPERTIES OF MOTOR UNITS , 1985 .

[14]  R. Enoka,et al.  The 1- to 2-Hz oscillations in muscle force are exacerbated by stress, especially in older adults. , 2004, Journal of applied physiology.

[15]  D. Farina,et al.  Fluctuations in isometric muscle force can be described by one linear projection of low‐frequency components of motor unit discharge rates , 2009, The Journal of physiology.

[16]  J. R. Rosenberg,et al.  Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans , 1998, Neuroscience Letters.

[17]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[18]  J. Dempsey,et al.  Role of respiratory motor output in within-breath modulation of muscle sympathetic nerve activity in humans. , 1999, Circulation research.

[19]  M. Hallett,et al.  Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism , 1999, Clinical Neurophysiology.

[20]  D. Vaillancourt,et al.  Force dysmetria in spinocerebellar ataxia 6 correlates with functional capacity , 2015, Front. Hum. Neurosci..

[21]  N. Stergiou,et al.  Human movement variability, nonlinear dynamics, and pathology: is there a connection? , 2011, Human movement science.

[22]  J. Cauraugh,et al.  Force control improvements in chronic stroke: bimanual coordination and motor synergy evidence after coupled bimanual movement training , 2014, Experimental Brain Research.

[23]  C. D. De Luca,et al.  Behaviour of human motor units in different muscles during linearly varying contractions , 1982, The Journal of physiology.

[24]  Jose Luis Patino,et al.  Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output , 2007, NeuroImage.

[25]  E. Christou,et al.  Age-Associated Differences in Positional Variability Are Greater With the Lower Limb , 2011, Journal of motor behavior.

[26]  Kris S Chaisanguanthum,et al.  Motor Variability Arises from a Slow Random Walk in Neural State , 2014, The Journal of Neuroscience.

[27]  K. Newell,et al.  Noise, information transmission, and force variability. , 1999, Journal of experimental psychology. Human perception and performance.

[28]  E. Christou,et al.  Increased voluntary drive is associated with changes in common oscillations from 13 to 60 Hz of interference but not rectified electromyography , 2010, Muscle & nerve.

[29]  M. Hallett,et al.  Corticomuscular coherence: a review. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[30]  Ajay S. Kurani,et al.  Functional Brain Activity Relates to 0-3 and 3-8 Hz Force Oscillations in Essential Tremor. , 2015, Cerebral cortex.

[31]  Les G Carlton,et al.  Modeling Variability of Force During Isometric Contractions of the Quadriceps Femoris , 2002, Journal of motor behavior.

[32]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[33]  D. Vaillancourt,et al.  Greater amount of visual feedback decreases force variability by reducing force oscillations from 0–1 and 3–7 Hz , 2010, European Journal of Applied Physiology.

[34]  J. Cauraugh,et al.  Force control in chronic stroke , 2015, Neuroscience & Biobehavioral Reviews.

[35]  J. Cauraugh,et al.  Increased Force Variability in Chronic Stroke: Contributions of Force Modulation below 1 Hz , 2013, PloS one.

[36]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[37]  Daniel M. Wolpert,et al.  Making smooth moves , 2022 .

[38]  K. Newell,et al.  Intermittency in the control of continuous force production. , 2000, Journal of neurophysiology.

[39]  C. D. De Luca,et al.  Control scheme governing concurrently active human motor units during voluntary contractions , 1982, The Journal of physiology.

[40]  T. Ebner,et al.  Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. , 2004, Journal of neurophysiology.

[41]  R. Kristeva-Feige,et al.  Effects of attention and precision of exerted force on beta range EEG-EMG synchronization during a maintained motor contraction task , 2002, Clinical Neurophysiology.

[42]  Evangelos A. Christou,et al.  Aging and Variability of Voluntary Contractions , 2011, Exercise and sport sciences reviews.

[43]  A. Mark,et al.  Effects of the cold pressor test on muscle sympathetic nerve activity in humans. , 1987, Hypertension.

[44]  R. Callister,et al.  Sympathetic activity is influenced by task difficulty and stress perception during mental challenge in humans. , 1992, The Journal of physiology.

[45]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[46]  N. A. Bernshteĭn The co-ordination and regulation of movements , 1967 .

[47]  M. Shinohara,et al.  Oscillations in motor unit discharge are reflected in the low-frequency component of rectified surface EMG and the rate of change in force , 2013, Experimental Brain Research.

[48]  R. Lemon,et al.  Human Cortical Muscle Coherence Is Directly Related to Specific Motor Parameters , 2000, The Journal of Neuroscience.

[49]  H. Zelaznik,et al.  Motor-output variability: a theory for the accuracy of rapid motor acts. , 1979, Psychological review.

[50]  Mark L. Latash,et al.  The bliss (not the problem) of motor abundance (not redundancy) , 2012, Experimental Brain Research.