Neural bases of hand synergies

The human hand has so many degrees of freedom that it may seem impossible to control. A potential solution to this problem is “synergy control” which combines dimensionality reduction with great flexibility. With applicability to a wide range of tasks, this has become a very popular concept. In this review, we describe the evolution of the modern concept using studies of kinematic and force synergies in human hand control, neurophysiology of cortical and spinal neurons, and electromyographic (EMG) activity of hand muscles. We go beyond the often purely descriptive usage of synergy by reviewing the organization of the underlying neuronal circuitry in order to propose mechanistic explanations for various observed synergy phenomena. Finally, we propose a theoretical framework to reconcile important and still debated concepts such as the definitions of “fixed” vs. “flexible” synergies and mechanisms underlying the combination of synergies for hand control.

[1]  C. Sherrington Flexion‐reflex of the limb, crossed extension‐reflex, and reflex stepping and standing , 1910, The Journal of physiology.

[2]  J. Napier The prehensile movements of the human hand. , 1956, The Journal of bone and joint surgery. British volume.

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

[4]  G. J. Thomas The Co-ordination and Regulation of Movements , 1967 .

[5]  O. Oscarsson Functional Organization of Spinocerebellar Paths , 1973 .

[6]  M. Sanders Handbook of Sensory Physiology , 1975 .

[7]  P. Kirkwood On the use and interpretation of cross-correlation measurements in the mammalian central nervous system , 1979, Journal of Neuroscience Methods.

[8]  E. Fetz,et al.  Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. , 1980, Journal of neurophysiology.

[9]  J. Yokota,et al.  Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey , 1981, Neuroscience Letters.

[10]  J Inukai,et al.  Principles of motor organization of the monkey cervical spinal cord , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. Elliott,et al.  A CLASSIFICATION OF MANIPULATIVE HAND MOVEMENTS , 1984, Developmental medicine and child neurology.

[12]  E. Fetz,et al.  Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: evidence for functional groups of CM cells. , 1985, Journal of neurophysiology.

[13]  E. Fetz,et al.  Patterns of facilitation and suppression of antagonist forelimb muscles from motor cortex sites in the awake monkey. , 1985, Journal of neurophysiology.

[14]  M. Illert,et al.  Location of motoneurones projecting to the cat distal forelimb. II. Median and ulnar motornuclei , 1986, The Journal of comparative neurology.

[15]  M. Illert,et al.  Location of motoneurones projecting to the cat distal forelimb. I. Deep radial motornuclei , 1986, The Journal of comparative neurology.

[16]  R. Lemon,et al.  Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. , 1986, The Journal of physiology.

[17]  M. Arbib,et al.  Opposition Space as a Structuring Concept for the Analysis of Skilled Hand Movements , 1986 .

[18]  R. Lemon,et al.  The influence of changes in discharge frequency of corticospinal neurones on hand muscles in the monkey. , 1989, The Journal of physiology.

[19]  Mark R. Cutkosky,et al.  On grasp choice, grasp models, and the design of hands for manufacturing tasks , 1989, IEEE Trans. Robotics Autom..

[20]  J F Soechting,et al.  Kinematics of typing: parallel control of the two hands. , 1992, Journal of neurophysiology.

[21]  E. Jankowska Interneuronal relay in spinal pathways from proprioceptors , 1992, Progress in Neurobiology.

[22]  PL Strick,et al.  Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  M. Schieber,et al.  How somatotopic is the motor cortex hand area? , 1993, Science.

[24]  J F Soechting,et al.  The learning of novel finger movement sequences. , 1994, Journal of neurophysiology.

[25]  R. Lemon,et al.  The influence of single monkey cortico‐motoneuronal cells at different levels of activity in target muscles. , 1994, The Journal of physiology.

[26]  Richard M. Murray,et al.  A Mathematical Introduction to Robotic Manipulation , 1994 .

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

[28]  Moshe Hershkovitz,et al.  Experimental validation of an optimization formulation of the human grasping quality sense , 1997, J. Field Robotics.

[29]  J F Soechting,et al.  Matching object size by controlling finger span and hand shape. , 1997, Somatosensory & motor research.

[30]  Moshe Hershkovitz,et al.  Experimental validation of an optimization formulation of the human grasping quality sense , 1997, J. Field Robotics.

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

[32]  E. Fetz,et al.  Response patterns and force relations of monkey spinal interneurons during active wrist movement. , 1998, Journal of neurophysiology.

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

[34]  F. Zajac,et al.  Large index-fingertip forces are produced by subject-independent patterns of muscle excitation. , 1998, Journal of biomechanics.

[35]  E. Fetz,et al.  Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey. , 1998, Journal of neurophysiology.

[36]  Marc H Schieber,et al.  Multiple fragment statistical analysis of post-spike effects in spike-triggered averages of rectified EMG , 1998, Journal of Neuroscience Methods.

[37]  M. Latash,et al.  Force sharing among fingers as a model of the redundancy problem , 1998, Experimental Brain Research.

[38]  P. Cheney,et al.  Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. , 1998, Journal of neurophysiology.

[39]  Gregor Schöner,et al.  The uncontrolled manifold concept: identifying control variables for a functional task , 1999, Experimental Brain Research.

[40]  M. Schieber,et al.  Limited functional grouping of neurons in the motor cortex hand area during individuated finger movements: A cluster analysis. , 1999, Journal of neurophysiology.

[41]  E. Fetz,et al.  Primate spinal interneurons show pre-movement instructed delay activity , 1999, Nature.

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

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

[44]  M. Latash,et al.  Enslaving effects in multi-finger force production , 2000, Experimental Brain Research.

[45]  K. Reilly,et al.  Independence of force production by digits of the human hand , 2000, Neuroscience Letters.

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

[47]  J. R. Rosenberg,et al.  On the application, estimation and interpretation of coherence and pooled coherence , 2000, Journal of Neuroscience Methods.

[48]  J. F. Soechting,et al.  Two virtual fingers in the control of the tripod grasp. , 2001, Journal of neurophysiology.

[49]  H. Hultborn State‐dependent modulation of sensory feedback , 2001, The Journal of physiology.

[50]  M. Latash,et al.  Structure of motor variability in marginally redundant multifinger force production tasks , 2001, Experimental Brain Research.

[51]  W. Mrówczyński,et al.  Neurones in the cervical enlargement of the cat spinal cord antidromically activated from sacral segments and the inferior cerebellar peduncle , 2001, Neuroscience Research.

[52]  Carolyn R. Mason,et al.  Hand synergies during reach-to-grasp. , 2001, Journal of neurophysiology.

[53]  P. Brown,et al.  EEG–EMG, MEG–EMG and EMG–EMG frequency analysis: physiological principles and clinical applications , 2002, Clinical Neurophysiology.

[54]  S. Votaw,et al.  Roles of primate spinal interneurons in preparation and execution of voluntary hand movement , 2002, Brain Research Reviews.

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

[56]  M. Latash,et al.  Prehension synergies: Effects of object geometry and prescribed torques , 2002, Experimental Brain Research.

[57]  Michael I. Jordan,et al.  Optimal feedback control as a theory of motor coordination , 2002, Nature Neuroscience.

[58]  Silvestro Micera,et al.  On the analysis of hand synergies during grasping in weightlessness. , 2002, Journal of gravitational physiology : a journal of the International Society for Gravitational Physiology.

[59]  M. Santello,et al.  Force synergies for multifingered grasping: effect of predictability in object center of mass and handedness , 2002, Experimental Brain Research.

[60]  Gregor Schöner,et al.  A mode hypothesis for finger interaction during multi-finger force-production tasks , 2003, Biological Cybernetics.

[61]  S. Grillner The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

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

[63]  R. Enoka,et al.  Motor-unit coherence during isometric contractions is greater in a hand muscle of older adults. , 2003, Journal of neurophysiology.

[64]  David J. Ostry,et al.  A critical evaluation of the force control hypothesis in motor control , 2003, Experimental Brain Research.

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

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

[67]  M. Santello,et al.  The role of vision on hand preshaping during reach to grasp , 2003, Experimental Brain Research.

[68]  Luis F. Schettino,et al.  Effects of object shape and visual feedback on hand configuration during grasping , 2003, Experimental Brain Research.

[69]  M. Schieber,et al.  Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. , 2003, Journal of neurophysiology.

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

[71]  Fan Gao,et al.  Matrix analyses of interaction among fingers in static force production tasks , 2003, Biological Cybernetics.

[72]  M. Latash,et al.  Prehension synergies: trial-to-trial variability and hierarchical organization of stable performance , 2003, Experimental Brain Research.

[73]  M. Latash,et al.  Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without Down syndrome , 2003, Experimental Brain Research.

[74]  Fan Gao,et al.  Finger force vectors in multi-finger prehension. , 2003, Journal of biomechanics.

[75]  K. Reilly,et al.  Human handedness: is there a difference in the independence of the digits on the preferred and non-preferred hands? , 2004, Experimental Brain Research.

[76]  Carolyn R. Mason,et al.  Monkey hand postural synergies during reach-to-grasp in the absence of vision of the hand and object. , 2004, Journal of neurophysiology.

[77]  T Brochier,et al.  Patterns of muscle activity underlying object-specific grasp by the macaque monkey. , 2004, Journal of neurophysiology.

[78]  Marc H Schieber,et al.  Hand function: peripheral and central constraints on performance. , 2004, Journal of applied physiology.

[79]  C. Ekerot The lateral reticular nucleus in the cat , 2004, Experimental Brain Research.

[80]  Luis F. Schettino,et al.  Deficits in the evolution of hand preshaping in Parkinson’s disease , 2004, Neuropsychologia.

[81]  Xudong Zhang,et al.  Quantitative analysis of finger motion coordination in hand manipulative and gestic acts. , 2004, Human movement science.

[82]  S. Sasaki,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[83]  S. Kitazawa,et al.  Candidate premotor neurones of skin reflex pathways to T1 forelimb motoneurones of the cat , 2004, Experimental Brain Research.

[84]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[85]  R. Enoka,et al.  Quantification of the factors that influence discharge correlation in model motor neurons. , 2004, Journal of neurophysiology.

[86]  Fethi Ben Ouezdou,et al.  Muscle forces prediction of the human hand and forearm system in highly realistic simulation , 2004, 2004 IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS) (IEEE Cat. No.04CH37566).

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

[88]  Y. Shinoda,et al.  Spinal branching of pyramidal tract neurons in the monkey , 1979, Experimental Brain Research.

[89]  O. Oscarsson,et al.  The lateral reticular nucleus in the cat I. Mossy fibre distribution in cerebellar cortex , 2004, Experimental Brain Research.

[90]  J. F. Soechting,et al.  Use of tactile afferent information in sequential finger movements , 2004, Experimental Brain Research.

[91]  E. Todorov,et al.  Analysis of the synergies underlying complex hand manipulation , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[92]  J. F. Soechting,et al.  Non-uniform temporal scaling of hand and finger kinematics during typing , 1993, Experimental Brain Research.

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

[94]  A. Lundberg,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 1977, Experimental Brain Research.

[95]  C. Ekerot The lateral reticular nucleus in the cat , 2004, Experimental Brain Research.

[96]  Todd C. Pataky,et al.  Prehension synergies during nonvertical grasping, II: Modeling and optimization , 2004, Biological Cybernetics.

[97]  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.

[98]  M. Latash,et al.  Learning multi-finger synergies: an uncontrolled manifold analysis , 2004, Experimental Brain Research.

[99]  Martha Flanders,et al.  Flexibility and Repeatability of Finger Movements During Typing: Analysis of Multiple Degrees of Freedom , 1997, Journal of Computational Neuroscience.

[100]  Marco Santello,et al.  Common input to motor units of digit flexors during multi-digit grasping. , 2004, Journal of neurophysiology.

[101]  O. Oscarsson,et al.  The lateral reticular nucleus in the cat III. Organization of component activated from ipsilateral forelimb tract , 2004, Experimental Brain Research.

[102]  Halla B. Olafsdottir,et al.  Is the thumb a fifth finger? A study of digit interaction during force production tasks , 2004, Experimental Brain Research.

[103]  J. F. Soechting,et al.  Synergistic finger movements in a skilled motor task , 2004, Experimental Brain Research.

[104]  H. Asanuma,et al.  Projection of individual pyramidal tract neurons to lumbar motor nuclei of the monkey , 1979, Experimental Brain Research.

[105]  Martha Flanders,et al.  Muscular and postural synergies of the human hand. , 2004, Journal of neurophysiology.

[106]  Peter K. Allen,et al.  Graspit! A versatile simulator for robotic grasping , 2004, IEEE Robotics & Automation Magazine.

[107]  Luis F. Schettino,et al.  Hand preshaping in Parkinson’s disease: effects of visual feedback and medication state , 2005, Experimental Brain Research.

[108]  A. Fuglevand,et al.  Common Input across Motor Nuclei Mediating Precision Grip in Humans , 2005, The Journal of Neuroscience.

[109]  C. Moritz,et al.  Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. , 2005, Journal of neurophysiology.

[110]  Scott L. Delp,et al.  A Model of the Upper Extremity for Simulating Musculoskeletal Surgery and Analyzing Neuromuscular Control , 2005, Annals of Biomedical Engineering.

[111]  M. Santello,et al.  Periodic modulation of motor-unit activity in extrinsic hand muscles during multidigit grasping. , 2005, Journal of neurophysiology.

[112]  T. Ebner,et al.  Finger movements during reach-to-grasp in the monkey: amplitude scaling of a temporal synergy , 2006, Experimental Brain Research.

[113]  J. F. Soechting,et al.  Modulation of grasping forces during object transport. , 2005, Journal of neurophysiology.

[114]  M. Santello,et al.  Effects of end-goal on hand shaping. , 2006, Journal of neurophysiology.

[115]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[116]  Andrea d'Avella,et al.  Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. , 2006, Journal of neurophysiology.

[117]  J. F. Soechting,et al.  Anticipatory and sequential motor control in piano playing , 1997, Experimental Brain Research.

[118]  M. Santello,et al.  Muscle-pair specific distribution and grip-type modulation of neural common input to extrinsic digit flexors. , 2006, Journal of neurophysiology.

[119]  B. Alstermark,et al.  Properties of propriospinal neurons in the C3-C4 segments mediating disynaptic pyramidal excitation to forelimb motoneurons in the macaque monkey. , 2006, Journal of neurophysiology.

[120]  E. G. Cruz,et al.  Impact of finger posture on mapping from muscle activation to joint torque. , 2006, Clinical biomechanics.

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

[122]  Marco Santello,et al.  Choice of Contact Points during Multidigit Grasping: Effect of Predictability of Object Center of Mass Location , 2007, The Journal of Neuroscience.

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

[124]  M. Turvey Action and perception at the level of synergies. , 2007, Human movement science.

[125]  S. Sasaki,et al.  Direct and indirect cortico-motoneuronal pathways and control of hand/arm movements. , 2007, Physiology.

[126]  S. Sasaki,et al.  The C3–C4 propriospinal system in the cat and monkey: a spinal pre‐motoneuronal centre for voluntary motor control , 2007, Acta physiologica.

[127]  Luca Turella,et al.  An object for an action, the same object for other actions: effects on hand shaping , 2008, Experimental Brain Research.

[128]  T. Flash,et al.  Task-Dependent Selection of Grasp Kinematics and Stiffness in Human Object Manipulation , 2007, Cortex.

[129]  Anatol G. Feldman,et al.  Threshold position control of arm movement with anticipatory increase in grip force , 2007, Experimental Brain Research.

[130]  M. Flanders,et al.  Timing of muscle activation in a hand movement sequence. , 2006, Cerebral cortex.

[131]  A. Georgopoulos,et al.  Mapping of the preferred direction in the motor cortex , 2007, Proceedings of the National Academy of Sciences.

[132]  Mingui Sun,et al.  Time-Varying Synergies in Velocity Profiles of Finger Joints of the Hand during Reach and Grasp , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[133]  J. Soechting,et al.  Multidigit control of contact forces during transport of handheld objects. , 2007, Journal of neurophysiology.

[134]  M. Schieber,et al.  Partial reconstruction of muscle activity from a pruned network of diverse motor cortex neurons. , 2007, Journal of neurophysiology.

[135]  E. Bizzi,et al.  Article history: , 2005 .

[136]  M. Santello,et al.  Anticipatory Control of Grasping: Independence of Sensorimotor Memories for Kinematics and Kinetics , 2008, The Journal of Neuroscience.

[137]  M. Latash,et al.  Effects of grasping force magnitude on the coordination of digit forces in multi-finger prehension , 2009, Experimental Brain Research.

[138]  Amy J Bastian,et al.  Multidigit Movement Synergies of the Human Hand in an Unconstrained Haptic Exploration Task , 2008, The Journal of Neuroscience.

[139]  Zhi-Hong Mao,et al.  Inherent bimanual postural synergies in hands , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[140]  Sun Wook Kim,et al.  Finger inter-dependence: linking the kinetic and kinematic variables. , 2008, Human Movement Science.

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

[142]  M. Santello,et al.  Common input to motor units of intrinsic and extrinsic hand muscles during two-digit object hold. , 2008, Journal of neurophysiology.

[143]  K. Seki,et al.  Spinomuscular coherence in monkeys performing a precision grip task. , 2008, Journal of neurophysiology.

[144]  Sun Wook Kim,et al.  Prehension synergies and control with referent hand configurations , 2010, Experimental Brain Research.

[145]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[146]  S. Baker,et al.  Renshaw Cell Recurrent Inhibition Improves Physiological Tremor by Reducing Corticomuscular Coupling at 10 Hz , 2009, The Journal of Neuroscience.

[147]  R. Rosenfeld Synergy , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[148]  Wei Wang,et al.  Quantizing and characterizing the variance of hand postures in a novel transformation task , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[149]  Luis F. Schettino,et al.  Deep Brain Stimulation of the Subthalamic Nucleus Facilitates Coordination of Hand Preshaping in Parkinson's Disease , 2009, The International journal of neuroscience.

[150]  M. Tresch,et al.  The case for and against muscle synergies , 2022 .

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

[152]  Emanuel Todorov,et al.  Structured variability of muscle activations supports the minimal intervention principle of motor control. , 2009, Journal of neurophysiology.

[153]  Matei T. Ciocarlie,et al.  Functional analysis of finger contact locations during grasping , 2009, World Haptics 2009 - Third Joint EuroHaptics conference and Symposium on Haptic Interfaces for Virtual Environment and Teleoperator Systems.

[154]  G. Loeb,et al.  Spinal-Like Regulator Facilitates Control of a Two-Degree-of-Freedom Wrist , 2010, The Journal of Neuroscience.

[155]  M. Santello,et al.  Anticipatory Planning and Control of Grasp Positions and Forces for Dexterous Two-Digit Manipulation , 2010, The Journal of Neuroscience.

[156]  Zhi-Hong Mao,et al.  Temporal Postural Synergies of the Hand in Rapid Grasping Tasks , 2010, IEEE Transactions on Information Technology in Biomedicine.

[157]  Marco Santello,et al.  Force-independent distribution of correlated neural inputs to hand muscles during three-digit grasping. , 2010, Journal of neurophysiology.

[158]  K. Seki,et al.  Spinal Interneurons Facilitate Coactivation of Hand Muscles during a Precision Grip Task in Monkeys , 2010, The Journal of Neuroscience.

[159]  Mark L Latash,et al.  An analytical approach to the problem of inverse optimization with additive objective functions: an application to human prehension , 2010, Journal of mathematical biology.

[160]  T. M. Hamm,et al.  Influence of fatigue on hand muscle coordination and EMG-EMG coherence during three-digit grasping. , 2010, Journal of neurophysiology.

[161]  T. M. Hamm,et al.  Assessment of across-muscle coherence using multi-unit vs. single-unit recordings , 2010, Experimental Brain Research.

[162]  U. Castiello,et al.  Testing the effects of end-goal during reach-to-grasp movements in Parkinson’s disease , 2010, Brain and Cognition.

[163]  M. Santello,et al.  Coordination of intrinsic and extrinsic hand muscle activity as a function of wrist joint angle during two-digit grasping , 2010, Neuroscience Letters.

[164]  Zhi-Hong Mao,et al.  Dimensionality Reduction in Control and Coordination of the Human Hand , 2008, IEEE Transactions on Biomedical Engineering.

[165]  Marco Santello,et al.  Transfer of Learned Manipulation following Changes in Degrees of Freedom , 2011, The Journal of Neuroscience.

[166]  Heiner Deubel,et al.  Contact points during multidigit grasping of geometric objects , 2011, Experimental Brain Research.

[167]  Martha Flanders,et al.  Coordination of Hand Shape , 2011, The Journal of Neuroscience.

[168]  Antonio Bicchi,et al.  Modelling natural and artificial hands with synergies , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[169]  B. Alstermark,et al.  Motor command for precision grip in the macaque monkey can be mediated by spinal interneurons. , 2011, Journal of neurophysiology.

[170]  Marco Santello,et al.  The effects of task and content on digit placement on a bottle , 2011, Experimental Brain Research.

[171]  Antonio Bicchi,et al.  On the role of hand synergies in the optimal choice of grasping forces , 2010, Auton. Robots.

[172]  Silvia Arber,et al.  Motor Circuits in Action: Specification, Connectivity, and Function , 2012, Neuron.

[173]  D. Watanabe,et al.  Genetic dissection of the circuit for hand dexterity in primates , 2012, Nature.

[174]  Simon A. Overduin,et al.  Microstimulation Activates a Handful of Muscle Synergies , 2012, Neuron.

[175]  Marco Santello,et al.  Synergistic Control of Hand Muscles Through Common Neural Input , 2014, The Human Hand as an Inspiration for Robot Hand Development.