Muscular and postural synergies of the human hand.

Because humans have limited ability to independently control the many joints of the hand, a wide variety of hand shapes can be characterized as a weighted combination of just two or three main patterns of covariation in joint rotations, or "postural synergies." The present study sought to align muscle synergies with these main postural synergies and to describe the form of membership of motor units in these postural/muscle synergies. Seventeen joint angles and the electromyographic (EMG) activities of several hand muscles (both intrinsic and extrinsic muscles) were recorded while human subjects held the hand statically in 52 specific shapes (i.e., shaping the hand around 26 commonly grasped objects or forming the 26 letter shapes of a manual alphabet). Principal-components analysis revealed several patterns of muscle synergy, some of which represented either coactivation of all hand muscles, or reciprocal patterns of activity (above and below average levels) in the intrinsic index finger and thumb muscles or (to a lesser extent) in the extrinsic four-tendoned extensor and flexor muscles. Single- and multiunit activity was generally a multimodal function of whole hand shape. This implies that motor-unit activation does not align with a single synergy; instead, motor units participate in multiple muscle synergies. Thus it appears that the organization of the global pattern of hand muscle activation is highly distributed. This organization mirrors the highly fractured somatotopy of cortical hand representations and may provide an ideal substrate for motor learning and recovery from injury.

[1]  D. F. Collins,et al.  Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand. , 1996, The Journal of physiology.

[2]  U Herrmann,et al.  Directional Tuning of Single Motor Units , 1998, The Journal of Neuroscience.

[3]  Martha Flanders,et al.  Choosing a wavelet for single-trial EMG , 2002, Journal of Neuroscience Methods.

[4]  Frédéric Albert,et al.  Proprioceptive population coding of limb position in humans , 2003, Experimental Brain Research.

[5]  S. Schäfer,et al.  The acceleration response of a primary muscle-spindle ending to ramp stretch of the extrafusal muscle , 1967, Experientia.

[6]  C. Gielen,et al.  Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks , 1984, Experimental Neurology.

[7]  Marco Santello,et al.  Task-dependent modulation of multi-digit force coordination patterns. , 2003, Journal of neurophysiology.

[8]  F J Valero-Cuevas,et al.  Activation patterns of the thumb muscles during stable and unstable pinch tasks. , 2001, The Journal of hand surgery.

[9]  M. Jeannerod,et al.  Influence of object position and size on human prehension movements , 1997, Experimental Brain Research.

[10]  K. Reilly,et al.  Incomplete functional subdivision of the human multitendoned finger muscle flexor digitorum profundus: an electromyographic study. , 2003, Journal of neurophysiology.

[11]  D A Robinson,et al.  The use of control systems analysis in the neurophysiology of eye movements. , 1981, Annual review of neuroscience.

[12]  R. Johansson,et al.  Control of grip force during restraint of an object held between finger and thumb: responses of muscle and joint afferents from the digits , 2004, Experimental Brain Research.

[13]  R. Griffiths,et al.  Roles of muscle activity and load on the relationship between muscle spindle length and whole muscle length in the freely walking cat. , 1989, Progress in brain research.

[14]  C. C. A. M. Gielen,et al.  The relation between the direction dependence of electromyographic amplitude and motor unit recruitment thresholds during isometric contractions , 1994, Experimental Brain Research.

[15]  U. Proske Stretch-evoked potentiation of responses of muscle spindles in the cat , 1975, Brain Research.

[16]  B. Edin Cutaneous afferents provide information about knee joint movements in humans , 2001, The Journal of physiology.

[17]  A. Fuglevand,et al.  Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. , 2004, Journal of neurophysiology.

[18]  B. Edin Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. , 1992, Journal of neurophysiology.

[20]  T J Roberts,et al.  Muscular Force in Running Turkeys: The Economy of Minimizing Work , 1997, Science.

[21]  M. Schieber Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[22]  Mikael Bergenheim,et al.  The preferred sensory direction of muscle spindle primary endings influences the velocity coding of two-dimensional limb movements in humans , 2002, Experimental Brain Research.

[23]  B. Edin,et al.  Skin strain patterns provide kinaesthetic information to the human central nervous system. , 1995, The Journal of physiology.

[24]  G E Loeb,et al.  The computation of position sense from spindles in mono- and multiarticular muscles , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  R. Johansson,et al.  Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits , 1996, Experimental Brain Research.

[26]  J. F. Soechting,et al.  Biological constraints simplify the recognition of hand shapes , 2003, IEEE Transactions on Biomedical Engineering.

[27]  A. Vallbo,et al.  Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. , 1968, Experimental neurology.

[28]  D. Elliot,et al.  The Excursions of the Long Extensor Tendons of the Hand , 1986, Journal of hand surgery.

[29]  R S Johansson,et al.  Sensory input and control of grip. , 1998, Novartis Foundation symposium.

[30]  M Hulliger,et al.  The effects of fusimotor stimulation during small amplitude stretching on the frequency‐response of the primary ending of the mammalian muscle spindle. , 1975, The Journal of physiology.

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

[32]  K. An,et al.  Mechanical advantage of the thumb muscles. , 1998, Journal of biomechanics.

[33]  M. Hallett,et al.  Velocity sensitivity of human muscle spindle afferents and slowly adapting type II cutaneous mechanoreceptors. , 1995, The Journal of physiology.

[34]  S. Hsiao,et al.  Representation of object size in the somatosensory system. , 2006, Journal of neurophysiology.

[35]  A. Lundberg,et al.  The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. , 1967, Acta physiologica Scandinavica.

[36]  J. Abbs,et al.  Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. , 1991, Journal of neurophysiology.

[37]  R. Johansson,et al.  Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip , 2004, Experimental Brain Research.

[38]  Mikael Bergenheim,et al.  Proprioceptive population coding of two-dimensional limb movements in humans: II. Muscle-spindle feedback during "drawing-like" movements , 2000, Experimental Brain Research.

[39]  F. Valero-Cuevas Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range. , 2000, Journal of neurophysiology.

[40]  A B Vallbo,et al.  Stretch sensitization of human muscle spindles. , 1988, The Journal of physiology.

[41]  Constantinos N Maganaris,et al.  Active, non‐spring‐like muscle movements in human postural sway: how might paradoxical changes in muscle length be produced? , 2005, The Journal of physiology.

[42]  M. Flanders,et al.  Two components of muscle activation: scaling with the speed of arm movement. , 1992, Journal of neurophysiology.

[43]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[44]  S. Gandevia,et al.  Change in length of relaxed muscle fascicles and tendons with knee and ankle movement in humans , 2002, The Journal of physiology.

[45]  Benoni B. Edin,et al.  Single unit retrieval in microneurography: a microprocessor-based device controlled by an operator , 1988, Journal of Neuroscience Methods.

[46]  B. Edin Quantitative analyses of dynamic strain sensitivity in human skin mechanoreceptors. , 2004, Journal of neurophysiology.

[47]  J. F. Soechting,et al.  Gradual molding of the hand to object contours. , 1998, Journal of neurophysiology.

[48]  Responses of human muscle spindle afferents during isotonic position holding and active movements , 1990, Brain Research.

[49]  J. F. Soechting,et al.  Postural Hand Synergies for Tool Use , 1998, The Journal of Neuroscience.

[50]  Erhard J. Huesler,et al.  EMG activation patterns during force production in precision grip. III. Synchronisation of single motor units , 2000, Experimental Brain Research.

[51]  J. F. Soechting,et al.  Force synergies for multifingered grasping , 2000, Experimental Brain Research.

[52]  M. Hepp-Reymond,et al.  EMG activation patterns during force production in precision grip , 2004, Experimental Brain Research.

[53]  E. Luschei,et al.  Discharge of spindle afferents from jaw-closing muscles during chewing in alert monkeys. , 1975, Journal of neurophysiology.

[54]  I. Engberg,et al.  An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. , 1969, Acta physiologica Scandinavica.

[55]  R W Angel,et al.  Electromyography during voluntary movement: the two-burst pattern. , 1974, Electroencephalography and clinical neurophysiology.

[56]  MH Schieber Muscular production of individuated finger movements: the roles of extrinsic finger muscles , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  M. Hulliger,et al.  The absence of position response in spindle afferent units from human finger muscles during accurate position holding. , 1982, The Journal of physiology.

[58]  S. Gandevia,et al.  Limited independent flexion of the thumb and fingers in human subjects. , 1994, The Journal of physiology.

[59]  Bagrat Amirikian,et al.  Directional tuning profiles of motor cortical cells , 2000, Neuroscience Research.

[60]  P. Matthews,et al.  The central control of the dynamic response of muscle spindle receptors , 1962, The Journal of physiology.

[61]  P. Matthews,et al.  After‐effects of fusimotor stimulation on the response of muscle spindle primary afferent endings , 1969, The Journal of physiology.

[62]  B. Edin,et al.  Dynamic response of human muscle spindle afferents to stretch. , 1990, Journal of neurophysiology.

[63]  M Hulliger,et al.  Static and dynamic fusimotor action on the response of IA fibres to low frequency sinusoidal stretching of widely ranging amplitude , 1977, The Journal of physiology.

[64]  S. Gandevia,et al.  Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. , 2005, Journal of neurophysiology.

[65]  Jean-Pierre Roll,et al.  Proprioceptive population coding of two-dimensional limb movements in humans: I. Muscle spindle feedback during spatially oriented movements , 2000, Experimental Brain Research.

[66]  Emilio Bizzi,et al.  Combinations of muscle synergies in the construction of a natural motor behavior , 2003, Nature Neuroscience.

[67]  M H Schieber,et al.  Quantifying the Independence of Human Finger Movements: Comparisons of Digits, Hands, and Movement Frequencies , 2000, The Journal of Neuroscience.

[68]  S C Gandevia,et al.  Loop gain of reflexes controlling human standing measured with the use of postural and vestibular disturbances. , 1996, Journal of neurophysiology.

[69]  Do spindle afferents monitor joint position in man? A study with active position holding , 1981, Brain Research.

[70]  N. Kakuda Response of human muscle spindle afferents to sinusoidal stretching with a wide range of amplitudes , 2000, The Journal of physiology.

[71]  Marco Santello,et al.  Patterns of Hand Motion during Grasping and the Influence of Sensory Guidance , 2002, The Journal of Neuroscience.

[72]  A B Vallbo,et al.  Directional tuning of human forearm muscle afferents during voluntary wrist movements , 2001, The Journal of physiology.

[73]  J. F. Soechting,et al.  Coarticulation in Fluent Fingerspelling , 2003, The Journal of Neuroscience.

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