Do sensorimotor β-oscillations maintain muscle synergy representations in primary motor cortex?

Fries, 2009, Neuronal gamma-band synchronization as a fundamental process in cortical computation, Annu. Rev. Neurosci., 32, 209, 10.1146/annurev.neuro.051508.135603 Senkowski, 2008, Crossmodal binding through neural coherence: implications for multisensory processing, Trends Neurosci., 31, 401, 10.1016/j.tins.2008.05.002 Jensen, 2007, Human gamma-frequency oscillations associated with attention and memory, Trends Neurosci., 30, 317, 10.1016/j.tins.2007.05.001 Palva, 2007, New vistas for alpha-frequency band oscillations, Trends Neurosci., 30, 150, 10.1016/j.tins.2007.02.001 Buzsaki, 2004, Neuronal oscillations in cortical networks, Science, 304, 1926, 10.1126/science.1099745 Siegel, 2012, Spectral fingerprints of large-scale neuronal interactions, Nat. Rev. Neurosci., 13, 121, 10.1038/nrn3137 Lisman, 2013, The theta-gamma neural code, Neuron, 77, 1002, 10.1016/j.neuron.2013.03.007 Engel, 2010, Beta-band oscillations – signalling the status quo?, Curr. Opin. Neurobiol., 20, 156, 10.1016/j.conb.2010.02.015 Murthy, 1996, Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior, J. Neurophysiol., 76, 3949, 10.1152/jn.1996.76.6.3949 Fetz, 2000, Synaptic interactions mediating synchrony and oscillations in primate sensorimotor cortex, J. Physiol. Paris, 94, 323, 10.1016/S0928-4257(00)01089-5 Classen, 1998, Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain, J. Neurophysiol., 79, 1567, 10.1152/jn.1998.79.3.1567 Baker, 1999, The role of synchrony and oscillations in the motor output, Exp. Brain Res., 128, 109, 10.1007/s002210050825 Baker, 1997, Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation, J. Physiol., 501, 225, 10.1111/j.1469-7793.1997.225bo.x Brown, 2000, Cortical drives to human muscle: the Piper and related rhythms, Prog. Neurobiol., 60, 97, 10.1016/S0301-0082(99)00029-5 Donoghue, 1998, Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements, J. Neurophysiol., 79, 159, 10.1152/jn.1998.79.1.159 Mackay, 1997, Synchronized neuronal oscillations and their role in motor processes, Trends Cogn. Sci., 1, 176, 10.1016/S1364-6613(97)01059-0 Sanes, 1993, Oscillations in local field potentials of the primate motor cortex during voluntary movement, Proc. Natl. Acad. Sci. U.S.A., 90, 4470, 10.1073/pnas.90.10.4470 Brovelli, 2004, Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality, Proc. Natl. Acad. Sci. U.S.A., 101, 9849, 10.1073/pnas.0308538101 Witham, 2007, Network oscillations and intrinsic spiking rhythmicity do not covary in monkey sensorimotor areas, J. Physiol., 580, 801, 10.1113/jphysiol.2006.124503 Murthy, 1992, Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys, Proc. Natl. Acad. Sci. U.S.A., 89, 5670, 10.1073/pnas.89.12.5670 Murthy, 1996, Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys, J. Neurophysiol., 76, 3968, 10.1152/jn.1996.76.6.3968 Salenius, 1997, Cortical control of human motoneuron firing during isometric contraction, J. Neurophysiol., 77, 3401, 10.1152/jn.1997.77.6.3401 Takei, 2008, Spinomuscular coherence in monkeys performing a precision grip task, J. Neurophysiol., 99, 2012, 10.1152/jn.01181.2007 Kilner, 2004, Coupling of oscillatory activity between muscles is strikingly reduced in a deafferented subject compared with normal controls, J. Neurophysiol., 92, 790, 10.1152/jn.01247.2003 Baker, 2007, Oscillatory interactions between sensorimotor cortex and the periphery, Curr. Opin. Neurobiol., 17, 649, 10.1016/j.conb.2008.01.007 Kilner, 1999, Task-dependent modulation of 15–30Hz coherence between rectified EMGs from human hand and forearm muscles, J. Physiol., 516, 559, 10.1111/j.1469-7793.1999.0559v.x Baker, 2006, Afferent encoding of central oscillations in the monkey arm, J. Neurophysiol., 95, 3904, 10.1152/jn.01106.2005 Soteropoulos, 2006, Cortico-cerebellar coherence during a precision grip task in the monkey, J. Neurophysiol., 95, 1194, 10.1152/jn.00935.2005 Aumann, 2004, Oscillatory activity in forelimb muscles of behaving monkeys evoked by microstimulation in the cerebellar nuclei, Neurosci. Lett., 361, 106, 10.1016/j.neulet.2003.12.091 Courtemanche, 2003, Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys, J. Neurosci., 23, 11741, 10.1523/JNEUROSCI.23-37-11741.2003 Witham, 2007, Cells in somatosensory areas show synchrony with beta oscillations in monkey motor cortex, Eur. J. Neurosci., 26, 2677, 10.1111/j.1460-9568.2007.05890.x van Ede, 2011, Orienting attention to an upcoming tactile event involves a spatially and temporally specific modulation of sensorimotor alpha- and beta-band oscillations, J. Neurosci., 31, 2016, 10.1523/JNEUROSCI.5630-10.2011 Halliday, 1998, Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans, Neurosci. Lett., 241, 5, 10.1016/S0304-3940(97)00964-6 Conway, 1995, Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man, J. Physiol., 489, 917, 10.1113/jphysiol.1995.sp021104 Farmer, 1993, The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man, J. Physiol., 470, 127, 10.1113/jphysiol.1993.sp019851 Witham, 2011, Contributions of descending and ascending pathways to corticomuscular coherence in humans, J. Physiol., 589, 3789, 10.1113/jphysiol.2011.211045 Mima, 2000, Electroencephalographic measurement of motor cortex control of muscle activity in humans, Clin. Neurophysiol., 111, 326, 10.1016/S1388-2457(99)00229-1 Salenius, 1997, Modulation of human cortical rolandic rhythms during natural sensorimotor tasks, Neuroimage, 5, 221, 10.1006/nimg.1997.0261 Jackson, 2002, Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation, J. Physiol., 541, 685, 10.1113/jphysiol.2001.015099 Fisher, 2002, Digital nerve anaesthesia decreases EMG-EMG coherence in a human precision grip task, Exp. Brain Res., 145, 207, 10.1007/s00221-002-1113-x Pohja, 2003, Modulation of cortex-muscle oscillatory interaction by ischaemia-induced deafferentation, Neuroreport, 14, 321, 10.1097/00001756-200303030-00005 Riddle, 2005, Manipulation of peripheral neural feedback loops alters human corticomuscular coherence, J. Physiol., 566, 625, 10.1113/jphysiol.2005.089607 Gerloff, 2006, Coherent corticomuscular oscillations originate from primary motor cortex: evidence from patients with early brain lesions, Hum. Brain Mapp., 27, 789, 10.1002/hbm.20220 Cheney, 1984, Corticomotoneuronal cells contribute to long-latency stretch reflexes in the rhesus monkey, J. Physiol., 349, 249, 10.1113/jphysiol.1984.sp015155 Jami, 1985, Activation of cat muscle spindles by static skeletofusimotor axons, J. Physiol., 369, 323, 10.1113/jphysiol.1985.sp015904 Gray, 1996, Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex, Science, 274, 109, 10.1126/science.274.5284.109 Wang, 2010, Neurophysiological and computational principles of cortical rhythms in cognition, Physiol. Rev., 90, 1195, 10.1152/physrev.00035.2008 Chen, 2005, Characteristic membrane potential trajectories in primate sensorimotor cortex neurons recorded in vivo, J. Neurophysiol., 94, 2713, 10.1152/jn.00024.2005 van Ede, 2013, Somatosensory demands modulate muscular Beta oscillations, independent of motor demands, J. Neurosci., 33, 10849, 10.1523/JNEUROSCI.5629-12.2013 Averbeck, 2004, Coding and transmission of information by neural ensembles, Trends Neurosci., 27, 225, 10.1016/j.tins.2004.02.006 Schieber, 2001, Constraints on somatotopic organization in the primary motor cortex, J. Neurophysiol., 86, 2125, 10.1152/jn.2001.86.5.2125 Fetz, 1980, Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells, J. Neurophysiol., 44, 751, 10.1152/jn.1980.44.4.751 Shinoda, 1981, Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey, Neurosci. Lett., 23, 7, 10.1016/0304-3940(81)90182-8 Landry, 1980, Intracortical distribution of axonal collaterals of pyramidal tract cells in the cat motor cortex, Brain Res., 191, 327, 10.1016/0006-8993(80)91284-6 Keller, 1993, Synaptic relationships involving local axon collaterals of pyramidal neurons in the cat motor cortex, J. Comp. Neurol., 336, 229, 10.1002/cne.903360206 Donoghue, 1992, Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles, Exp. Brain Res., 89, 1, 10.1007/BF00228996 McKiernan, 1998, Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task, J. Neurophysiol., 80, 1961, 10.1152/jn.1998.80.4.1961 Griffin, 2009, Stability of output effects from motor cortex to forelimb muscles in primates, J. Neurosci., 29, 1915, 10.1523/JNEUROSCI.4831-08.2009 Adelsberger, 2014, Local domains of motor cortical activity revealed by fiber-optic calcium recordings in behaving nonhuman primates, Proc. Natl. Acad. Sci. U.S.A., 111, 463, 10.1073/pnas.1321612111 Holdefer, 2002, Primary motor cortical neurons encode functional muscle synergies, Exp. Brain Res., 146, 233, 10.1007/s00221-002-1166-x Kargo, 2003, Early skill learning is expressed through selection and tuning of cortically represented muscle synergies, J. Neurosci., 23, 11255, 10.1523/JNEUROSCI.23-35-11255.2003 Kirsch, 2014, Primary motor cortex neurons during individuated finger and wrist movements: correlation of spike firing rates with the motion of individual digits versus their principal components, Front. Neurol., 5, 10.3389/fneur.2014.00070 Overduin, 2014, Muscle synergies evoked by microstimulation are preferentially encoded during behavior, Front. Comput. Neurosci., 8, 10.3389/fncom.2014.00020 Graziano, 2007, Mapping behavioral repertoire onto the cortex, Neuron, 56, 239, 10.1016/j.neuron.2007.09.013 Dottori, 1998, EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract, Proc. Natl. Acad. Sci. U.S.A., 95, 13248, 10.1073/pnas.95.22.13248 Hsu, 2005, Temporal and spatial distribution of growth-associated molecules and astroglial cells in the rat corticospinal tract during development, J. Neurosci. Res., 80, 330, 10.1002/jnr.20472 Shim, 2012, Cis-regulatory control of corticospinal system development and evolution, Nature, 486, 74, 10.1038/nature11094 Chakrabarty, 2009, Activity-dependent plasticity improves M1 motor representation and corticospinal tract connectivity, J. Neurophysiol., 101, 1283, 10.1152/jn.91026.2008 Martin, 2007, Activity- and use-dependent plasticity of the developing corticospinal system, Neurosci. Biobehav. Rev., 31, 1125, 10.1016/j.neubiorev.2007.04.017 Chakrabarty, 2005, Motor but not sensory representation in motor cortex depends on postsynaptic activity during development and in maturity, J. Neurophysiol., 94, 3192, 10.1152/jn.00424.2005 Kleim, 2003, Functional organization of adult motor cortex is dependent upon continued protein synthesis, Neuron, 40, 167, 10.1016/S0896-6273(03)00592-0 Nudo, 1996, Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys, J. Neurosci., 16, 785, 10.1523/JNEUROSCI.16-02-00785.1996 Nudo, 2001, Role of adaptive plasticity in recovery of function after damage to motor cortex, Muscle Nerve, 24, 1000, 10.1002/mus.1104 Sanes, 2000, Plasticity and primary motor cortex, Annu. Rev. Neurosci., 23, 393, 10.1146/annurev.neuro.23.1.393 Van Dongen, 2003, The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation, Sleep, 26, 117, 10.1093/sleep/26.2.117 Walker, 2004, Sleep-dependent learning and memory consolidation, Neuron, 44, 121, 10.1016/j.neuron.2004.08.031 Milner, 1974, A model for visual shape recognition, Psychol. Rev., 81, 521, 10.1037/h0037149 Abeles, 1982 Von der Malsburg, 1981, The correlation theory of brain function, 95 Singer, 1993, Synchronization of cortical activity and its putative role in information processing and learning, Annu. Rev. Physiol., 55, 349, 10.1146/annurev.ph.55.030193.002025 Engel, 1992, Temporal coding in the visual cortex: new vistas on integration in the nervous system, Trends Neurosci., 15, 218, 10.1016/0166-2236(92)90039-B Eckhorn, 1988, Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat, Biol. Cybern., 60, 121, 10.1007/BF00202899 Pienkowski, 2011, Cortical tonotopic map plasticity and behavior, Neurosci. Biobehav. Rev., 35, 2117, 10.1016/j.neubiorev.2011.02.002 Wespatat, 2004, Phase sensitivity of synaptic modifications in oscillating cells of rat visual cortex, J. Neurosci., 24, 9067, 10.1523/JNEUROSCI.2221-04.2004 Schieber, 2002, Training and synchrony in the motor system, J. Neurosci., 22, 5277, 10.1523/JNEUROSCI.22-13-05277.2002 Omlor, 2011, Corticospinal beta-range coherence is highly dependent on the pre-stationary motor state, J. Neurosci., 31, 8037, 10.1523/JNEUROSCI.4153-10.2011