Common muscle synergies for balance and walking

Little is known about the integration of neural mechanisms for balance and locomotion. Muscle synergies have been studied independently in standing balance and walking, but not compared. Here, we hypothesized that reactive balance and walking are mediated by a common set of lower-limb muscle synergies. In humans, we examined muscle activity during multidirectional support-surface perturbations during standing and walking, as well as unperturbed walking at two speeds. We show that most muscle synergies used in perturbations responses during standing were also used in perturbation responses during walking, suggesting common neural mechanisms for reactive balance across different contexts. We also show that most muscle synergies using in reactive balance were also used during unperturbed walking, suggesting that neural circuits mediating locomotion and reactive balance recruit a common set of muscle synergies to achieve task-level goals. Differences in muscle synergies across conditions reflected differences in the biomechanical demands of the tasks. For example, muscle synergies specific to walking perturbations may reflect biomechanical challenges associated with single limb stance, and muscle synergies used during sagittal balance recovery in standing but not walking were consistent with maintaining the different desired center of mass motions in standing vs. walking. Thus, muscle synergies specifying spatial organization of muscle activation patterns may define a repertoire of biomechanical subtasks available to different neural circuits governing walking and reactive balance and may be recruited based on task-level goals. Muscle synergy analysis may aid in dissociating deficits in spatial vs. temporal organization of muscle activity in motor deficits. Muscle synergy analysis may also provide a more generalizable assessment of motor function by identifying whether common modular mechanisms are impaired across the performance of multiple motor tasks.

[1]  J. Andrew Pruszynski,et al.  Primary motor cortex underlies multi-joint integration for fast feedback control , 2011, Nature.

[2]  William J Kargo,et al.  Individual Premotor Drive Pulses, Not Time-Varying Synergies, Are the Units of Adjustment for Limb Trajectories Constructed in Spinal Cord , 2008, The Journal of Neuroscience.

[3]  A. M. Degtyarenko,et al.  Patterns of locomotor drive to motoneurons and last-order interneurons: clues to the structure of the CPG. , 2001, Journal of neurophysiology.

[4]  A.E. Patla,et al.  Strategies for dynamic stability during adaptive human locomotion , 2003, IEEE Engineering in Medicine and Biology Magazine.

[5]  S. Rossignol,et al.  The locomotion of the low spinal cat. II. Interlimb coordination. , 1980, Acta physiologica Scandinavica.

[6]  Torrence D. J. Welch,et al.  A feedback model explains the differential scaling of human postural responses to perturbation acceleration and velocity. , 2009, Journal of neurophysiology.

[7]  G. Courtine,et al.  Human walking along a curved path. II. Gait features and EMG patterns , 2003, The European journal of neuroscience.

[8]  S. Giszter,et al.  Modular Premotor Drives and Unit Bursts as Primitives for Frog Motor Behaviors , 2004, The Journal of Neuroscience.

[9]  N.V. Thakor,et al.  Decoding Individuated Finger Movements Using Volume-Constrained Neuronal Ensembles in the M1 Hand Area , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[10]  K. Pearson,et al.  Corrective responses to loss of ground support during walking. II. Comparison of intact and chronic spinal cats. , 1994, Journal of neurophysiology.

[11]  J. A. Pruszynski,et al.  Optimal feedback control and the long-latency stretch response , 2012, Experimental Brain Research.

[12]  E E Fetz,et al.  Corticomotoneuronal cells contribute to long‐latency stretch reflexes in the rhesus monkey. , 1984, The Journal of physiology.

[13]  C. Marsden,et al.  Human postural responses. , 1981, Brain : a journal of neurology.

[14]  Stacie A. Chvatal,et al.  Voluntary and Reactive Recruitment of Locomotor Muscle Synergies during Perturbed Walking , 2012, The Journal of Neuroscience.

[15]  C E Coogler,et al.  The effect of Tai Chi Quan and computerized balance training on postural stability in older subjects. Atlanta FICSIT Group. Frailty and Injuries: Cooperative Studies on Intervention Techniques. , 1997, Physical therapy.

[16]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

[17]  M. Woollacott,et al.  Control of reactive balance adjustments in perturbed human walking: roles of proximal and distal postural muscle activity , 1998, Experimental Brain Research.

[18]  M. Gorassini,et al.  Corrective responses to loss of ground support during walking. I. Intact cats. , 1994, Journal of neurophysiology.

[19]  R. Gentner,et al.  Encoding of Motor Skill in the Corticomuscular System of Musicians , 2010, Current Biology.

[20]  Julia A. Leonard,et al.  Postural responses to unexpected perturbations of balance during reaching , 2010, Experimental Brain Research.

[21]  A. Berthoz,et al.  Head stabilization during various locomotor tasks in humans , 2004, Experimental Brain Research.

[22]  S. Grillner Locomotion in vertebrates: central mechanisms and reflex interaction. , 1975, Physiological reviews.

[23]  D. McCrea,et al.  Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provide clues to the organization of the mammalian central pattern generator. , 2005, Journal of neurophysiology.

[24]  Tadashi Isa,et al.  Circuits for skilled reaching and grasping. , 2012, Annual review of neuroscience.

[25]  Francesco Lacquaniti,et al.  Control of Fast-Reaching Movements by Muscle Synergy Combinations , 2006, The Journal of Neuroscience.

[26]  T. Drew,et al.  Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat , 2002, Brain Research Reviews.

[27]  L. Miller,et al.  Primary motor cortical neurons encode functional muscle synergies , 2002, Experimental Brain Research.

[28]  Mark G. Carpenter,et al.  Directional sensitivity of stretch reflexes and balance corrections for normal subjects in the roll and pitch planes , 1999, Experimental Brain Research.

[29]  Reed Ferber,et al.  Reactive balance adjustments to unexpected perturbations during human walking. , 2002, Gait & posture.

[30]  J. Misiaszek Early activation of arm and leg muscles following pulls to the waist during walking , 2003, Experimental Brain Research.

[31]  Emilio Bizzi,et al.  Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors. , 2009, Journal of neurophysiology.

[32]  T. G. Deliagina,et al.  Spinal and supraspinal postural networks , 2008, Brain Research Reviews.

[33]  J. Duysens,et al.  Muscle reflexes and synergies triggered by an unexpected support surface height during walking. , 2007, Journal of neurophysiology.

[34]  L. Ting,et al.  Muscle synergies characterizing human postural responses. , 2007, Journal of neurophysiology.

[35]  F. Horak,et al.  Postural Orientation and Equilibrium , 2011 .

[36]  Lena H Ting,et al.  Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts. , 2010, Journal of neurophysiology.

[37]  Hannah J. Block,et al.  Interlimb coordination during locomotion: what can be adapted and stored? , 2005, Journal of neurophysiology.

[38]  J. Kalaska,et al.  Muscle synergies during locomotion in the cat: a model for motor cortex control , 2008, The Journal of physiology.

[39]  E. Bizzi,et al.  Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors , 2005, The Journal of Neuroscience.

[40]  Claire F. Honeycutt,et al.  Bilateral impairments in task-dependent modulation of the long-latency stretch reflex following stroke , 2013, Clinical Neurophysiology.

[41]  D. McCrea,et al.  Organization of mammalian locomotor rhythm and pattern generation , 2008, Brain Research Reviews.

[42]  Ilse Jonkers,et al.  The flexion synergy, mother of all synergies and father of new models of gait , 2013, Front. Comput. Neurosci..

[43]  Francesco Lacquaniti,et al.  Superposition and modulation of muscle synergies for reaching in response to a change in target location. , 2011, Journal of neurophysiology.

[44]  Eric J. Perreault,et al.  Stretch sensitive reflexes as an adaptive mechanism for maintaining limb stability , 2010, Clinical Neurophysiology.

[45]  Lena H Ting,et al.  Neuromechanics of muscle synergies for posture and movement , 2007, Current Opinion in Neurobiology.

[46]  H. Sebastian Seung,et al.  Learning the parts of objects by non-negative matrix factorization , 1999, Nature.

[47]  F. Lacquaniti,et al.  Coordination of Locomotion with Voluntary Movements in Humans , 2005, The Journal of Neuroscience.

[48]  Dario Farina,et al.  Modular organization of balance control following perturbations during walking. , 2012, Journal of neurophysiology.

[49]  Dario Farina,et al.  Identifying representative synergy matrices for describing muscular activation patterns during multidirectional reaching in the horizontal plane. , 2010, Journal of neurophysiology.

[50]  R. Cham,et al.  Slip-related muscle activation patterns in the stance leg during walking. , 2007, Gait & posture.

[51]  A Pouget,et al.  Decoding M1 neurons during multiple finger movements. , 2007, Journal of neurophysiology.

[52]  Marc H Schieber,et al.  Bilateral Spike-Triggered Average Effects in Arm and Shoulder Muscles from the Monkey Pontomedullary Reticular Formation , 2007, The Journal of Neuroscience.

[53]  Jean Saunders,et al.  Getting the Balance Right: A randomised controlled trial of physiotherapy and Exercise Interventions for ambulatory people with multiple sclerosis , 2009, BMC neurology.

[54]  J M Macpherson,et al.  Weight support and balance during perturbed stance in the chronic spinal cat. , 1999, Journal of neurophysiology.

[55]  T. Drew,et al.  Sequential activation of motor cortical neurons contributes to intralimb coordination during reaching in the cat by modulating muscle synergies. , 2011, Journal of neurophysiology.

[56]  F. Su,et al.  Effect of slip on movement of body center of mass relative to base of support. , 2001, Clinical biomechanics.

[57]  Richard R Neptune,et al.  Modular control of human walking: Adaptations to altered mechanical demands. , 2010, Journal of biomechanics.

[58]  Stacie A. Chvatal,et al.  Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors. , 2011, Journal of neurophysiology.

[59]  C. Heckman,et al.  Intrinsic electrical properties of spinal motoneurons vary with joint angle , 2007, Nature Neuroscience.

[60]  Arun Ramakrishnan,et al.  A simple experimentally based model using proprioceptive regulation of motor primitives captures adjusted trajectory formation in spinal frogs. , 2010, Journal of neurophysiology.

[61]  S. Giszter,et al.  A Neural Basis for Motor Primitives in the Spinal Cord , 2010, The Journal of Neuroscience.

[62]  T. Brown The intrinsic factors in the act of progression in the mammal , 1911 .

[63]  Lena H Ting,et al.  A limited set of muscle synergies for force control during a postural task. , 2005, Journal of neurophysiology.

[64]  V. Dietz,et al.  Vertical perturbations of human gait: organisation and adaptation of leg muscle responses , 2007, Experimental Brain Research.

[65]  F. Zajac,et al.  Locomotor strategy for pedaling: muscle groups and biomechanical functions. , 1999, Journal of neurophysiology.

[66]  D. B. Lockhart,et al.  Optimal sensorimotor transformations for balance , 2007, Nature Neuroscience.

[67]  V. Dietz,et al.  Interlimb coordination of leg-muscle activation during perturbation of stance in humans. , 1989, Journal of neurophysiology.

[68]  D. A. Brown,et al.  Phase reversal of biomechanical functions and muscle activity in backward pedaling. , 1999, Journal of neurophysiology.

[69]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.

[70]  Benjamin J. Fregly,et al.  Persons with Parkinson’s disease exhibit decreased neuromuscular complexity during gait , 2013, Clinical Neurophysiology.

[71]  Steven A. Kautz,et al.  Evaluation of Abnormal Synergy Patterns Poststroke: Relationship of the Fugl-Meyer Assessment to Hemiparetic Locomotion , 2010, Neurorehabilitation and neural repair.

[72]  Dario Farina,et al.  Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients. , 2011, Journal of neurophysiology.

[73]  Simon A. Overduin,et al.  Modulation of Muscle Synergy Recruitment in Primate Grasping , 2008, The Journal of Neuroscience.

[74]  Shinya Masahiro,et al.  Fast muscle responses to an unexpected foot-in-hole scenario, evoked in the context of prior knowledge of the potential perturbation , 2010, Experimental Brain Research.

[75]  T. Drew,et al.  Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. , 2008, Journal of neurophysiology.

[76]  Hillel J. Chiel,et al.  The Brain in Its Body: Motor Control and Sensing in a Biomechanical Context , 2009, The Journal of Neuroscience.

[77]  Conrad Wall,et al.  Recovery from perturbations during paced walking. , 2004, Gait & posture.

[78]  Richard R Neptune,et al.  Modular control of human walking: a simulation study. , 2009, Journal of biomechanics.

[79]  D A McCrea,et al.  Group I disynaptic excitation of cat hindlimb flexor and bifunctional motoneurones during fictive locomotion , 2000, The Journal of physiology.

[80]  Adam G. Davidson,et al.  Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging , 2006, Experimental Brain Research.

[81]  Richard R Neptune,et al.  Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. , 2010, Journal of neurophysiology.

[82]  E. Bizzi,et al.  The construction of movement by the spinal cord , 1999, Nature Neuroscience.

[83]  E. Bizzi,et al.  Modules in the brain stem and spinal cord underlying motor behaviors. , 2011, Journal of neurophysiology.

[84]  M. Bobbert,et al.  How early reactions in the support limb contribute to balance recovery after tripping. , 2005, Journal of biomechanics.

[85]  Lena H Ting,et al.  Dimensional reduction in sensorimotor systems: a framework for understanding muscle coordination of posture. , 2007, Progress in brain research.

[86]  F. Lacquaniti,et al.  Motor patterns in human walking and running. , 2006, Journal of neurophysiology.

[87]  Vengateswaran J Ravichandran,et al.  Contributions of altered stretch reflex coordination to arm impairments following stroke. , 2010, Journal of neurophysiology.

[88]  Stacie A. Chvatal,et al.  Decomposing Muscle Activity in Motor TasksMethods and Interpretation , 2010 .

[89]  T. Drew,et al.  Motor cortical cell discharge during voluntary gait modification , 1988, Brain Research.

[90]  J. Duysens,et al.  Significance of load receptor input during locomotion: a review. , 2000, Gait & posture.

[91]  J. Tanji,et al.  Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. , 1976, Journal of neurophysiology.

[92]  Steven L. Wolf,et al.  The Effect of Tai Chi Quan and Computerized Balance Training on Postural Stability in Older Subjects , 1997 .

[93]  S. Rossignol,et al.  Adaptive Mechanisms of Spinal Locomotion in Cats1 , 2004, Integrative and comparative biology.

[94]  Wolfgang Taube,et al.  Direct corticospinal pathways contribute to neuromuscular control of perturbed stance. , 2006, Journal of applied physiology.

[95]  N. A. Borghese,et al.  Kinematic determinants of human locomotion. , 1996, The Journal of physiology.

[96]  J. A. Pruszynski,et al.  Temporal evolution of "automatic gain-scaling". , 2009, Journal of neurophysiology.

[97]  L. Nashner Adapting reflexes controlling the human posture , 1976, Experimental Brain Research.

[98]  Lena H Ting,et al.  Muscle synergy organization is robust across a variety of postural perturbations. , 2006, Journal of neurophysiology.

[99]  Trevor Drew,et al.  Independent and convergent signals from the pontomedullary reticular formation contribute to the control of posture and movement during reaching in the cat. , 2004, Journal of neurophysiology.

[100]  Simon Giszter,et al.  Primitives, premotor drives, and pattern generation: a combined computational and neuroethological perspective. , 2007, Progress in brain research.

[101]  Joseph Classen,et al.  Modular Organization of Finger Movements by the Human Central Nervous System , 2006, Neuron.

[102]  Francesco Lacquaniti,et al.  Patterned control of human locomotion , 2012, The Journal of physiology.

[103]  J. Kalaska,et al.  Sequential activation of muscle synergies during locomotion in the intact cat as revealed by cluster analysis and direct decomposition. , 2006, Journal of neurophysiology.

[104]  T G Deliagina,et al.  Impairment of postural control in rabbits with extensive spinal lesions. , 2009, Journal of neurophysiology.

[105]  S. Rossignol,et al.  Locomotor capacities after complete and partial lesions of the spinal cord. , 1996, Acta neurobiologiae experimentalis.

[106]  Richard R Neptune,et al.  Three-dimensional modular control of human walking. , 2012, Journal of biomechanics.

[107]  Madeleine. E. Hackney,et al.  Effects of Dance on Gait and Balance in Parkinson’s Disease: A Comparison of Partnered and Nonpartnered Dance Movement , 2010, Neurorehabilitation and neural repair.

[108]  C. D. MARSDEN,et al.  Servo Action in Human Voluntary Movement , 1972, Nature.

[109]  Lena H Ting,et al.  Sensorimotor feedback based on task-relevant error robustly predicts temporal recruitment and multidirectional tuning of muscle synergies. , 2013, Journal of neurophysiology.

[110]  Emilio Bizzi,et al.  Shared and specific muscle synergies in natural motor behaviors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[111]  F E Zajac,et al.  Contralateral movement and extensor force generation alter flexion phase muscle coordination in pedaling. , 2000, Journal of neurophysiology.

[112]  Lena H Ting,et al.  Task-level feedback can explain temporal recruitment of spatially fixed muscle synergies throughout postural perturbations. , 2012, Journal of neurophysiology.

[113]  F. Horak,et al.  Central programming of postural movements: adaptation to altered support-surface configurations. , 1986, Journal of neurophysiology.

[114]  T. Nichols A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. , 1994, Acta anatomica.