Neuromechanics: an integrative approach for understanding motor control.

Neuromechanics seeks to understand how muscles, sense organs, motor pattern generators, and brain interact to produce coordinated movement, not only in complex terrain but also when confronted with unexpected perturbations. Applications of neuromechanics include ameliorating human health problems (including prosthesis design and restoration of movement following brain or spinal cord injury), as well as the design, actuation and control of mobile robots. In animals, coordinated movement emerges from the interplay among descending output from the central nervous system, sensory input from body and environment, muscle dynamics, and the emergent dynamics of the whole animal. The inevitable coupling between neural information processing and the emergent mechanical behavior of animals is a central theme of neuromechanics. Fundamentally, motor control involves a series of transformations of information, from brain and spinal cord to muscles to body, and back to brain. The control problem revolves around the specific transfer functions that describe each transformation. The transfer functions depend on the rules of organization and operation that determine the dynamic behavior of each subsystem (i.e., central processing, force generation, emergent dynamics, and sensory processing). In this review, we (1) consider the contributions of muscles, (2) sensory processing, and (3) central networks to motor control, (4) provide examples to illustrate the interplay among brain, muscles, sense organs and the environment in the control of movement, and (5) describe advances in both robotics and neuromechanics that have emerged from application of biological principles in robotic design. Taken together, these studies demonstrate that (1) intrinsic properties of muscle contribute to dynamic stability and control of movement, particularly immediately after perturbations; (2) proprioceptive feedback reinforces these intrinsic self-stabilizing properties of muscle; (3) control systems must contend with inevitable time delays that can simplify or complicate control; and (4) like most animals under a variety of circumstances, some robots use a trial and error process to tune central feedforward control to emergent body dynamics.

[1]  P. Aerts,et al.  Swimming and jumping in a semi-aquatic frog , 2005 .

[2]  T. Nichols Receptor mechanisms underlying heterogenic reflexes among the triceps surae muscles of the cat. , 1999, Journal of neurophysiology.

[3]  J. Pringle,et al.  The excitation and contraction of the flight muscles of insects , 1949, The Journal of physiology.

[4]  Elizabeth V. Mangan,et al.  A biologically inspired gripping device , 2005, Ind. Robot.

[5]  Jonathan E. Clark,et al.  Fast and Robust: Hexapedal Robots via Shape Deposition Manufacturing , 2002 .

[6]  Linda B. Smith,et al.  A Dynamic Systems Approach to the Development of Cognition and Action , 2007, Journal of Cognitive Neuroscience.

[7]  Elizabeth V. Mangan,et al.  Development of a peristaltic endoscope , 2002, Proceedings 2002 IEEE International Conference on Robotics and Automation (Cat. No.02CH37292).

[8]  Full,et al.  Static forces and moments generated in the insect leg: comparison of a three-dimensional musculo-skeletal computer model with experimental measurements , 1995, The Journal of experimental biology.

[9]  Melina E. Hale,et al.  In Vivo and Functional Imaging in Developmental Physiology , 2005 .

[10]  J. Eccles,et al.  The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones , 1957, The Journal of physiology.

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

[12]  R. Full,et al.  A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect. , 2002, The Journal of experimental biology.

[13]  H. Chiel,et al.  Activity patterns of the B31/B32 pattern initiators innervating the I2 muscle of the buccal mass during normal feeding movements in Aplysia californica. , 1996, Journal of neurophysiology.

[14]  Robert W. Gunderson,et al.  Unmanned Ground Vehicle Technology IV , 2000 .

[15]  R J Full,et al.  Distributed mechanical feedback in arthropods and robots simplifies control of rapid running on challenging terrain , 2007, Bioinspiration & biomimetics.

[16]  R. Beer,et al.  Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica , 2006, Journal of Comparative Physiology A.

[17]  J. V. van Leeuwen,et al.  Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development , 2004, Journal of Experimental Biology.

[18]  Roger D. Quinn,et al.  Design and simulation of a cockroach-like hexapod robot , 1997, Proceedings of International Conference on Robotics and Automation.

[19]  Roger D. Quinn,et al.  A hydrostatic robot for marine applications , 2000, Robotics Auton. Syst..

[20]  D A Kane,et al.  Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. , 1996, Development.

[21]  P. Aerts,et al.  Spatio-temporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus). , 2000, American journal of physical anthropology.

[22]  Sabine M P Verschueren,et al.  Position sensitivity of human muscle spindles: single afferent and population representations. , 2002, Journal of neurophysiology.

[23]  R. Blickhan,et al.  Similarity in multilegged locomotion: Bouncing like a monopode , 1993, Journal of Comparative Physiology A.

[24]  K. Edman,et al.  Maximum velocity of shortening related to myosin isoform composition in frog skeletal muscle fibres. , 1988, The Journal of physiology.

[25]  G. E. Loeb,et al.  A hierarchical foundation for models of sensorimotor control , 1999, Experimental Brain Research.

[26]  C. S. Carbonell The thoracic muscles of the cockroach Periplaneta americana (L.) , 1947 .

[27]  R. Full,et al.  Mechanical aspects of legged locomotion control. , 2004, Arthropod structure & development.

[28]  W. Kargo,et al.  Functional morphology of proximal hindlimb muscles in the frog Rana pipiens. , 2002, The Journal of experimental biology.

[29]  T L Hedrick,et al.  Flight control in the hawkmoth Manduca sexta: the inverse problem of hovering , 2006, Journal of Experimental Biology.

[30]  J. Houk,et al.  Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. , 1976, Journal of neurophysiology.

[31]  J. Jing,et al.  Interneuronal Basis of the Generation of Related but Distinct Motor Programs in Aplysia: Implications for Current Neuronal Models of Vertebrate Intralimb Coordination , 2002, The Journal of Neuroscience.

[32]  Roger D. Quinn,et al.  Insect Walking and Biorobotics: A Relationship with Mutual Benefits , 2000 .

[33]  J. Slotine,et al.  Intrinsic Musculoskeletal Properties Stabilize Wiping Movements in the Spinalized Frog , 2005, The Journal of Neuroscience.

[34]  G. Loeb,et al.  Electromyography for Experimentalists , 1986 .

[35]  K. Pearson,et al.  Innervation of coxal depressor muscles in the cockroach, Periplaneta americana. , 1971, The Journal of experimental biology.

[36]  Robert A. Harris,et al.  Adaptation and the temporal delay filter of fly motion detectors , 1999, Vision Research.

[37]  C. T. Farley,et al.  Human hopping on very soft elastic surfaces: implications for muscle pre-stretch and elastic energy storage in locomotion , 2005, Journal of Experimental Biology.

[38]  R. Full,et al.  Dynamics of geckos running vertically , 2006, Journal of Experimental Biology.

[39]  A. Biewener,et al.  Running over rough terrain: guinea fowl maintain dynamic stability despite a large unexpected change in substrate height , 2006, Journal of Experimental Biology.

[40]  V. Prince,et al.  Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. , 2002, Development.

[41]  Y. Arshavsky,et al.  Control of locomotion in marine mollusc Clione limacina IV. Role of type 12 interneurons , 2004, Experimental Brain Research.

[42]  R. Satterlie Reciprocal Inhibition and Postinhibitory Rebound Produce Reverberation in a Locomotor Pattern Generator , 1985, Science.

[43]  H. Chiel,et al.  Neuromechanics of Coordination during Swallowing in Aplysia californica , 2006, The Journal of Neuroscience.

[44]  A. Hill The heat of shortening and the dynamic constants of muscle , 1938 .

[45]  David R Corey,et al.  Morpholino antisense oligonucleotides: tools for investigating vertebrate development , 2001, Genome Biology.

[46]  Daniel A. Kingsley,et al.  A Cockroach Inspired Robot With Artificial Muscles , 2006, 2006 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[47]  R. Full,et al.  Dynamics of rapid vertical climbing in cockroaches reveals a template , 2006, Journal of Experimental Biology.

[48]  Randall D. Beer,et al.  The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment , 1997, Trends in Neurosciences.

[49]  R. Josephson Dissecting muscle power output. , 1999, The Journal of experimental biology.

[50]  Intrinsic properties and reflex compensation in reinnervated triceps surae muscles of the cat: effect of movement history. , 2003, Journal of neurophysiology.

[51]  H. Chiel,et al.  Neuromechanics of Multifunctionality during Rejection in Aplysia californica , 2006, The Journal of Neuroscience.

[52]  T. Nichols,et al.  Cross-bridge mechanisms underlying the history-dependent properties of muscle spindles and stretch reflexes. , 2004, Canadian journal of physiology and pharmacology.

[53]  J. Jing,et al.  Neural Mechanisms of Motor Program Switching inAplysia , 2001, The Journal of Neuroscience.

[54]  R. Satterlie,et al.  Cellular Mechanisms Underlying Swim Acceleration in the Pteropod Mollusk Clione limacina1 , 2004, Integrative and comparative biology.

[55]  Ian D. Walker,et al.  Field trials and testing of the OctArm continuum manipulator , 2006, Proceedings 2006 IEEE International Conference on Robotics and Automation, 2006. ICRA 2006..

[56]  J. D. Watson,et al.  Effect of vibrating agonist or antagonist muscle on the reflex response to sinusoidal displacement of the human forearm , 1981, The Journal of physiology.

[57]  R. Satterlie ELECTROPHYSIOLOGY OF SWIM MUSCULATURE IN THE PTEROPOD MOLLUSC CLIONE LIMACINA , 1991 .

[58]  P. Crago,et al.  Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing , 2004, Journal of Comparative Physiology A.

[59]  L. Jami Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. , 1992, Physiological reviews.

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

[61]  R. Enoka Neuromechanics of Human Movement , 2001 .

[62]  Sung-Nien Yu,et al.  Biomechanical properties and a kinetic simulation model of the smooth muscle I2 in the buccal mass of Aplysia , 1999, Biological Cybernetics.

[63]  J. Fetcho,et al.  The zebrafish space cadet gene controls axonal pathfinding of neurons that modulate fast turning movements. , 2001, Development.

[64]  Marc H. Raibert,et al.  Legged Robots That Balance , 1986, IEEE Expert.

[65]  G. Yamaguchi,et al.  Feeding Motor Patterns in Anurans: Insights from Biomechanical Modeling , 2001 .

[66]  T. Nichols,et al.  Intrinsic properties and reflex compensation in reinnervated triceps surae muscles of the cat: effect of activation level. , 2003, Journal of neurophysiology.

[67]  John Guckenheimer,et al.  The Dynamics of Legged Locomotion: Models, Analyses, and Challenges , 2006, SIAM Rev..

[68]  N. Cowan,et al.  Task-level control of rapid wall following in the American cockroach , 2006, Journal of Experimental Biology.

[69]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[70]  David W. Chestek,et al.  The kinematics of multifunctionality: comparisons of biting and swallowing in Aplysia californica , 2007, Journal of Experimental Biology.

[71]  R. Blickhan,et al.  Locomotion Energetics of the Ghost Crab: II. Mechanics of the Centre of Mass During Walking and Running , 1987 .

[72]  R. Quinn,et al.  Convergent evolution and locomotion through complex terrain by insects, vertebrates and robots. , 2004, Arthropod structure & development.

[73]  Randall D. Beer,et al.  Neural control exploits changing mechanical advantage and context dependence to generate different feeding responses in Aplysia , 2004, Biological Cybernetics.

[74]  J. Fulton,et al.  A NOTE CONCERNING THE PROBABLE FUNCTION OF VARIOUS AFFERENT END-ORGANS IN SKELETAL MUSCLE , 1928 .

[75]  C. T. Farley,et al.  Human hopping on damped surfaces: strategies for adjusting leg mechanics , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  P. Aerts,et al.  Lizard Locomotion: How Morphology Meets Ecology , 2000 .

[77]  Hillel J Chiel,et al.  Imaging freely moving subjects using continuous interleaved orthogonal magnetic resonance imaging. , 2004, Magnetic resonance imaging.

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

[79]  J. Houk,et al.  Sampling of total muscle force by tendon organs. , 1982, Journal of neurophysiology.

[80]  Robert J. Full,et al.  Biological Inspiration: Lessons from Many-Legged Locomotors , 2000 .

[81]  Daniel A. Kingsley,et al.  Fatigue life and frequency response of braided pneumatic actuators , 2002, Proceedings 2002 IEEE International Conference on Robotics and Automation (Cat. No.02CH37292).

[82]  T. Nichols,et al.  Movement reduces the dynamic response of muscle spindle afferents and motoneuron synaptic potentials in rat. , 2004, Journal of neurophysiology.

[83]  R. Full,et al.  In situ muscle power differs without varying in vitro mechanical properties in two insect leg muscles innervated by the same motor neuron , 2006, Journal of Experimental Biology.

[84]  Roger D. Quinn,et al.  Posture control of a cockroach-like robot , 1998, Proceedings. 1998 IEEE International Conference on Robotics and Automation (Cat. No.98CH36146).

[85]  A. Biewener,et al.  Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control , 2007, Journal of Experimental Biology.

[86]  A. Biewener,et al.  Patterns of strain and activation in the thigh muscles of goats across gaits during level locomotion , 2005, Journal of Experimental Biology.

[87]  D. Gardner The neurobiology of neural networks , 1993 .

[88]  H. Chiel,et al.  Neural architectures for adaptive behavior , 1994, Trends in Neurosciences.

[89]  Karsten Berns,et al.  Adaptive, neural control architecture for the walking machine LAURON , 1994, Proceedings of IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS'94).

[90]  H. Chiel,et al.  In vivo buccal nerve activity that distinguishes ingestion from rejection can be used to predict behavioral transitions in Aplysia , 1993, Journal of Comparative Physiology A.

[91]  R. Full,et al.  Dynamic stabilization of rapid hexapedal locomotion. , 2002, The Journal of experimental biology.

[92]  Malcolm Burrows,et al.  Biomechanics: Froghopper insects leap to new heights , 2003, Nature.

[93]  D A Kane,et al.  Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. , 1996, Development.

[94]  S. J. Arnold,et al.  Morphology, Performance and Fitness , 1983 .

[95]  A. Huxley,et al.  The maximum length for contraction in vertebrate striated muscle , 1961, The Journal of physiology.

[96]  B. R. Moon,et al.  The mechanics of swallowing and the muscular control of diverse behaviours in gopher snakes. , 2000, The Journal of experimental biology.

[97]  D. McCrea,et al.  Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. , 1995, The Journal of physiology.

[98]  P. Matthews The dependence of tension upon extension in the stretch reflex of the soleus muscle of the decerebrate cat , 1959, The Journal of physiology.

[99]  Roger D. Quinn,et al.  Transforming insect electromyograms into pneumatic muscle control , 2006, SPIE Defense + Commercial Sensing.

[100]  J. Houk,et al.  Function of the spindle dynamic response in stiffness regulation—a predictive mechanism provided by non-linear feedback , 1981 .

[101]  Full,et al.  Energy absorption during running by leg muscles in a cockroach , 1998, The Journal of experimental biology.

[102]  J. Eisen,et al.  Zebrafish deadly seven functions in neurogenesis. , 2001, Developmental biology.

[103]  R. Blickhan,et al.  Leg design in hexapedal runners. , 1991, The Journal of experimental biology.

[104]  Patrik Larsson,et al.  A Distributed Neural Network Architecture for Hexapod Robot Locomotion , 1992, Neural Computation.

[105]  K. Pearson,et al.  Enhancement and Resetting of Locomotor Activity by Muscle Afferentsa , 1998, Annals of the New York Academy of Sciences.

[106]  C G Evans,et al.  Characterization of a radula opener neuromuscular system in Aplysia. , 1996, Journal of neurophysiology.

[107]  R. Full,et al.  Mechanics of six-legged runners. , 1990, The Journal of experimental biology.

[108]  V. Prince,et al.  Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. , 2001, Development.

[109]  J. Houk,et al.  Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. , 1967, Journal of neurophysiology.

[110]  J. Fetcho,et al.  Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish , 1999, Neuron.

[111]  T A Abelew,et al.  Rapid spinal mechanisms of motor coordination. , 1999, Exercise and sport sciences reviews.

[112]  R.B. Stein,et al.  The role of neuromuscular properties in determining the end-point of a movement , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[113]  H. Chiel,et al.  Kinematics of the buccal mass during swallowing based on magnetic resonance imaging in intact, behaving Aplysia californica. , 2002, The Journal of experimental biology.

[114]  W. Kier,et al.  Functional morphology of the cephalopod buccal mass: A novel joint type , 2005, Journal of morphology.

[115]  Daniel E. Koditschek,et al.  Robotics in scansorial environments , 2005, SPIE Defense + Commercial Sensing.

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

[117]  M. Labarbera,et al.  Swimming in the pteropod mollusc, Clione limacina. I: Behaviour and morphology , 1985 .

[118]  Walter Herzog,et al.  Considerations on the history dependence of muscle contraction. , 2004, Journal of applied physiology.

[119]  Y. Arshavsky,et al.  Control of locomotion in marine mollusc Clione limacina III. On the origin of locomotory rhythm , 2004, Experimental Brain Research.

[120]  Ole Kiehn,et al.  Neuronal mechanisms for generating locomotor activity , 1998 .

[121]  P. Crago,et al.  A kinematic model of swallowing in Aplysia californica based on radula/odontophore kinematics and in vivo magnetic resonance images. , 2002, The Journal of experimental biology.

[122]  M. Dickinson,et al.  Wing rotation and the aerodynamic basis of insect flight. , 1999, Science.

[123]  S. Warburton Comparative developmental physiology : contributions, tools, and trends , 2006 .

[124]  Roger D. Quinn,et al.  Transforming Insect Electromyograms into Pneumatic Muscle Control , 2007, Proceedings 2007 IEEE International Conference on Robotics and Automation.

[125]  R. Ritzmann,et al.  Kinematics and motor activity during tethered walking and turning in the cockroach, Blaberus discoidalis , 2005, Journal of Comparative Physiology A.

[126]  R. Satterlie,et al.  SWIMMING IN THE PTEROPOD MOLLUSC, , 2005 .

[127]  M. S. Tu,et al.  Submaximal power output from the dorsolongitudinal flight muscles of the hawkmoth Manduca sexta , 2004, Journal of Experimental Biology.

[128]  M. Göpfert,et al.  The mechanical basis of Drosophila audition. , 2002, The Journal of experimental biology.

[129]  Blake Hannaford,et al.  Measurement and modeling of McKibben pneumatic artificial muscles , 1996, IEEE Trans. Robotics Autom..

[130]  J. Houk,et al.  Transition in sensitivity of spindle receptors that occurs when muscle is stretched more than a fraction of a millimeter. , 1975, Journal of neurophysiology.

[131]  P. Matthews,et al.  The sensitivity of muscle spindle afferents to small sinusoidal changes of length , 1969, The Journal of physiology.

[132]  R A Satterlie Neuromuscular organization in the swimming system of the pteropod mollusc Clione limacina. , 1993, The Journal of experimental biology.

[133]  R.D. Quinn,et al.  Design of a Quadruped Robot Driven by Air Muscles , 2006, The First IEEE/RAS-EMBS International Conference on Biomedical Robotics and Biomechatronics, 2006. BioRob 2006..

[134]  P. Aerts,et al.  Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus). , 2002, American journal of physical anthropology.

[135]  Andrew A Biewener,et al.  Running over rough terrain reveals limb control for intrinsic stability , 2006, Proceedings of the National Academy of Sciences.

[136]  Friedrich Pfeiffer,et al.  The Tum-Walking Machine , 1995, Intell. Autom. Soft Comput..

[137]  E. Bizzi,et al.  Motor systems , 1997, Current Opinion in Neurobiology.

[138]  A. Prochazka,et al.  Muscle Receptors and Movement , 1981, Palgrave Macmillan UK.

[139]  K. Edman,et al.  Length-tension-velocity relationships studied in short consecutive segments of intact muscle fibres of the frog. , 1984, Advances in experimental medicine and biology.

[140]  Rodney A. Brooks,et al.  A robot that walks; emergent behaviors from a carefully evolved network , 1989, Proceedings, 1989 International Conference on Robotics and Automation.

[141]  Kalmanje Krishnakumar,et al.  Micro-Genetic Algorithms For Stationary And Non-Stationary Function Optimization , 1990, Other Conferences.

[142]  A. Biewener,et al.  Muscle force-length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors , 2003, Journal of Experimental Biology.

[143]  A. Büschges Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. , 2005, Journal of neurophysiology.

[144]  A A Biewener,et al.  In Vivo and In Vitro Heterogeneity of Segment Length Changes in the Semimembranosus Muscle of the Toad , 2003, The Journal of physiology.

[145]  Daniel E. Koditschek,et al.  RHex: A Simple and Highly Mobile Hexapod Robot , 2001, Int. J. Robotics Res..

[146]  T. Nichols,et al.  The role of musculoskeletal mechanics in motor coordination. , 1999, Progress in brain research.

[147]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[148]  R. Satterlie,et al.  Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. I. Serotonin immunoreactivity in the central nervous system and wings. , 1995, The Journal of experimental biology.

[149]  Randall D. Beer,et al.  Biologically based distributed control and local reflexes improve rough terrain locomotion in a hexapod robot , 1996, Robotics Auton. Syst..

[150]  P. Stein,et al.  Step, swim, and scratch motor patterns in the turtle. , 2000, Journal of neurophysiology.

[151]  R. Alexander,et al.  Storage of elastic strain energy in muscle and other tissues , 1977, Nature.

[152]  A A Biewener,et al.  Muscle and Tendon Contributions to Force, Work, and Elastic Energy Savings: A Comparative Perspective , 2000, Exercise and sport sciences reviews.

[153]  Tigran P. Norekian,et al.  Mechanisms of Locomotory Speed Change: The Pteropod Solution1 , 2001 .

[154]  G A Pavlova,et al.  Control of locomotion in marine mollusc Clione limacina. VII Reexamination of type 12 interneurons. , 1989, Experimental brain research.

[155]  E. Gahtan,et al.  Evidence for a widespread brain stem escape network in larval zebrafish. , 2002, Journal of neurophysiology.

[156]  R. Josephson Mechanical Power output from Striated Muscle during Cyclic Contraction , 1985 .

[157]  Melina E. Hale,et al.  Swimming of larval zebrafish: fin–axis coordination and implications for function and neural control , 2004, Journal of Experimental Biology.

[158]  T. McMahon The role of compliance in mammalian running gaits. , 1985, The Journal of experimental biology.

[159]  H. Chiel,et al.  A new technique for chronic single-unit extracellular recording in freely behaving animals using pipette electrodes , 1995, Journal of Neuroscience Methods.

[160]  Darwin G. Caldwell,et al.  Control of pneumatic muscle actuators , 1995 .

[161]  Daniel Gardner Static determinants of synaptic strength , 1993 .

[162]  W. Rymer,et al.  Muscle stiffness during transient and continuous movements of cat muscle: perturbation characteristics and physiological relevance , 1994, IEEE Transactions on Biomedical Engineering.

[163]  Joel L. Davis,et al.  Neurotechnology for Biomimetic Robots , 2002 .

[164]  D. Faber,et al.  ■ Review : The Mauthner Cell: What Has it Taught us? , 2000 .

[165]  K. Pearson Proprioceptive regulation of locomotion , 1995, Current Opinion in Neurobiology.

[166]  K. Nishikawa,et al.  Storage and recovery of elastic potential energy powers ballistic prey capture in toads , 2006, Journal of Experimental Biology.

[167]  J. T. Watson,et al.  Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis : I. Slow running , 1997, Journal of Comparative Physiology A.

[168]  H. Cruse What mechanisms coordinate leg movement in walking arthropods? , 1990, Trends in Neurosciences.

[169]  Jack M. Winters,et al.  Biomechanics and Neural Control of Posture and Movement , 2011, Springer New York.

[170]  Melina E. Hale,et al.  A confocal study of spinal interneurons in living larval zebrafish , 2001, The Journal of comparative neurology.

[171]  Melina E. Hale,et al.  Hox Gene Misexpression and Cell-Specific Lesions Reveal Functionality of Homeotically Transformed Neurons , 2004, The Journal of Neuroscience.

[172]  J. Fetcho,et al.  Mutations in deadly seven/notch1a Reveal Developmental Plasticity in the Escape Response Circuit , 2003, The Journal of Neuroscience.

[173]  R. Blickhan,et al.  Dynamic and static stability in hexapedal runners. , 1994, The Journal of experimental biology.

[174]  T. McMahon,et al.  The mechanics of running: how does stiffness couple with speed? , 1990, Journal of biomechanics.

[175]  Robert J. Wood,et al.  Microrobotics using composite materials: the micromechanical flying insect thorax , 2003, 2003 IEEE International Conference on Robotics and Automation (Cat. No.03CH37422).

[176]  Topics in Functional and Ecological Vertebrate Morphology : Introduction , 2002 .

[177]  M. McGlamery Mammalian Muscle Receptors and Their Central Actions , 1973 .

[178]  D. O'Malley,et al.  Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. , 2000, The Journal of experimental biology.

[179]  Ian E. Brown,et al.  A Reductionist Approach to Creating and Using Neuromusculoskeletal Models , 2000 .

[180]  Helen Greiner,et al.  Autonomous legged underwater vehicles for near land warfare , 1996, Proceedings of Symposium on Autonomous Underwater Vehicle Technology.

[181]  R J Full,et al.  Templates and anchors: neuromechanical hypotheses of legged locomotion on land. , 1999, The Journal of experimental biology.

[182]  G. Cavagna,et al.  Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. , 1977, The American journal of physiology.

[183]  G. C. Joyce,et al.  The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements , 1969, The Journal of physiology.

[184]  A. Biewener Muscle Function in vivo: A Comparison of Muscles used for Elastic Energy Savings versus Muscles Used to Generate Mechanical Power1 , 1998 .

[185]  P. Aerts,et al.  Propulsive impulse as a covarying performance measure in the comparison of the kinematics of swimming and jumping in frogs , 2003, Journal of Experimental Biology.

[186]  K. Nishikawa Neuromuscular control of prey capture in frogs. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[187]  R J Full,et al.  How animals move: an integrative view. , 2000, Science.

[188]  G. N. Orlovsky,et al.  Control of locomotion in marine mollusc Clione limacina , 2004, Experimental Brain Research.

[189]  R. Satterlie,et al.  Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. III. Cerebral neurons. , 1995, The Journal of experimental biology.

[190]  A. Berkowitz Physiology and morphology indicate that individual spinal interneurons contribute to diverse limb movements. , 2005, Journal of neurophysiology.

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

[192]  A. Bianchi,et al.  Activation of XII motoneurons and premotor neurons during various oropharyngeal behaviors , 2005, Respiratory Physiology & Neurobiology.

[193]  K. Campbell,et al.  History-dependent mechanical properties of permeabilized rat soleus muscle fibers. , 2002, Biophysical journal.

[194]  G. E. Goslow,et al.  Two types of striated muscle suggest two‐geared swimming in the pteropod mollusc Clione limacina , 1990 .

[195]  Randall D. Beer,et al.  Leg Coordination Mechanisms in the Stick Insect Applied to Hexapod Robot Locomotion , 1993, Adapt. Behav..

[196]  M. Latash Neurophysiological basis of movement , 1998 .

[197]  Daniel Koditschek,et al.  Quantifying Dynamic Stability and Maneuverability in Legged Locomotion1 , 2002, Integrative and comparative biology.

[198]  R. Satterlie,et al.  Serotonin-induced spike narrowing in a locomotor pattern generator permits increases in cycle frequency during accelerations. , 2000, Journal of neurophysiology.

[199]  J. Prather,et al.  Central Suppression of Regenerated Proprioceptive Afferents , 2005, The Journal of Neuroscience.