Spikes alone do not behavior make: why neuroscience needs biomechanics
Open accessAbstract
Neural circuits do not function in isolation; they interact with the physical world, accepting sensory inputs and producing outputs via muscles. Since both these pathways are constrained by physics, the activity of neural circuits can only be understood by considering biomechanics of muscles, bodies, and the exterior world. We discuss how animal bodies have natural stable motions that require relatively little activation or control from the nervous system. The nervous system can substantially alter these motions, by subtly changing mechanical properties such as leg sti ness. Mechanics can also provide robustness to perturbations without sensory reflexes. By considering a complete neuromechanical system, neuroscientists and biomechanicians together can provide a more integrated view of neural circuitry and behavior.
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Cites
McGeer, T. (1990) · The International Journal of Robotics Research · doi:10.1177/027836499000900206 · Cited by 3,393 · see citing works
Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control.
Zajac, F. E. (1989) · PubMed · Cited by 2,980 · see citing works
Efficient Bipedal Robots Based on Passive-Dynamic Walkers
Collins, S. H., Ruina, A. L., Tedrake, R., & Wisse, M. (2005) · Science · doi:10.1126/science.1107799 · Cited by 1,878 · see citing works
How animals move: an integrative view
Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R., Kram, R., & Lehman, S. (2000) · Science · doi:10.1126/science.288.5463.100 · Cited by 1,633 · see citing works
The Kinematics and Performance of Fish Fast-Start Swimming
Domenici, P., & Blake, R. W. (1997) · Journal of Experimental Biology · doi:10.1242/jeb.200.8.1165 · Cited by 923 · see citing works
Chiel, H. J., & Beer, R. D. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01149-1 · Cited by 864 · see citing works
The aerodynamic effects of wing rotation and a revised quasi-steady model of flapping flight
Sane, S. P., & Dickinson, M. H. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.8.1087 · Cited by 779 · see citing works
Developing Maximal Neuromuscular Power: Part 1 – Biological Basis of Maximal Power Production
Cormie, P., McGuigan, M. R., & Newton, R. U. (2011) · Sports Medicine · doi:10.2165/11537690-000000000-00000 · Cited by 774 · see citing works
The Dynamics of Legged Locomotion: Models, Analyses, and Challenges
Holmes, P. J., Full, R. J., Koditschek, D., & Guckenheimer, J. M. (2006) · SIAM Review · doi:10.1137/s0036144504445133 · Cited by 708 · see citing works
Self-citationThe case for and against muscle synergies
Tresch, M. C., & Jarc, A. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.09.002 · Cited by 568 · see citing works
Direct cortical control of muscle activation in voluntary arm movements: a model
Todorov, E. (2000) · Nature Neuroscience · doi:10.1038/73964 · Cited by 439 · see citing works
The influence of track compliance on running
McMahon, T. A., & Greene, P. R. (1979) · Journal of Biomechanics · doi:10.1016/0021-9290(79)90057-5 · Cited by 362 · see citing works
A comparative analysis of actuator technologies for robotics
Hollerbach, J. M., Hunter, I. W., & Ballantyne, J. (1992) · Cited by 330 · see citing works
Tytell, E. D., Hsu, C.-Y., Williams, T. L., Cohen, A. H., & Fauci, L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011564107 · Cited by 300 · see citing works
Self-citationDynamic stabilization of rapid hexapedal locomotion
Jindrich, D. L., & Full, R. J. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.18.2803 · Cited by 286 · see citing works
Dielectric elastomer artificial muscle actuators: toward biomimetic motion
Pelrine, R., Kornbluh, R. D., Pei, Q., et al. (2002) · Proceedings of SPIE, the International Society for Optical Engineering/Proceedings of SPIE · doi:10.1117/12.475157 · Cited by 277 · see citing works
Horses damp the spring in their step
Wilson, A. M., McGuigan, M. P., Su, A., & van den Bogert, A. J. (2001) · Nature · doi:10.1038/414895a · Cited by 254 · see citing works
Muscle Efficiency and Elastic Storage in the Flight Motor of <i>Drosophila</i>
Dickinson, M. H., & Lighton, J. R. B. (1995) · Science · doi:10.1126/science.7701346 · Cited by 254 · see citing works
Dynamic and Static Stability in Hexapedal Runners
Ting, L. H., Blickhan, R., & Full, R. J. (1994) · Journal of Experimental Biology · doi:10.1242/jeb.197.1.251 · Cited by 240 · see citing works
Many-legged maneuverability: dynamics of turning in hexapods
Jindrich, D. L., & Full, R. J. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.12.1603 · Cited by 229 · see citing works
Sensitive dependence of the motion of a legged robot on granular media
Li, C., Umbanhowar, P. B., Komsuoḡlu, H., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809095106 · Cited by 216 · see citing works
Mechanical models for insect locomotion: dynamics and stability in the horizontal plane I. Theory
Schmitt, J., & Holmes, P. J. (2000) · Biological Cybernetics · doi:10.1007/s004220000181 · Cited by 207 · see citing works
Self-citationPassive wing pitch reversal in insect flight
Bergou, A. J., Xu, S., & Wang, Z. J. (2007) · Journal of Fluid Mechanics · doi:10.1017/s0022112007008440 · Cited by 203 · see citing works
A Reductionist Approach to Creating and Using Neuromusculoskeletal Models
Brown, I. E., & Loeb, G. E. (2000) · Springer eBooks · doi:10.1007/978-1-4612-2104-3_10 · Cited by 201 · see citing works
Implications of positive feedback in the control of movement.
Prochazka, A., Gillard, D. M., & Bennett, D. J. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3237 · Cited by 181 · see citing works
Simplified and effective motor control based on muscle synergies to exploit musculoskeletal dynamics
Berniker, M., Jarc, A., Bizzi, E., & Tresch, M. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901512106 · Cited by 179 · see citing works
Hydrodynamics of the escape response in bluegill sunfish,Lepomis macrochirus
Tytell, E. D., & LAUDER, G. V. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.020917 · Cited by 168 · see citing works
Self-citationFruit Flies Modulate Passive Wing Pitching to Generate In-Flight Turns
Bergou, A. J., Ristroph, L., Guckenheimer, J. M., Cohen, I., & Wang, Z. J. (2010) · Physical Review Letters · doi:10.1103/physrevlett.104.148101 · Cited by 168 · see citing works
Muscles, Elastic Energy, and the Dynamics of Body Stiffness in Swimming Eels
Long, J. H. (1998) · American Zoologist · doi:10.1093/icb/38.4.771 · Cited by 164 · see citing works
An Uncontrolled Walking Toy That Cannot Stand Still
Coleman, M. J., & Ruina, A. L. (1998) · Physical Review Letters · doi:10.1103/physrevlett.80.3658 · Cited by 158 · see citing works
Resonance Tuning in Rhythmic Arm Movements
Hatsopoulos, N. G., & Warren, W. H. (1996) · Journal of Motor Behavior · doi:10.1080/00222895.1996.9941728 · Cited by 148 · see citing works
Simulations of neuromuscular control in lamprey swimming
Ekeberg, Ö., & Grillner, S. (1999) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1999.0441 · Cited by 145 · see citing works
The Brain in its Body: Motor Control and Sensing in a Biomechanical Context
Chiel, H., Ting, L. H., Ekeberg, Ö., & Hartmann, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3338-09.2009 · Cited by 142 · see citing works
Phase Coupling by Synaptic Spread in Chains of Coupled Neuronal Oscillators
Williams, T. L. (1992) · Science · doi:10.1126/science.1411575 · Cited by 136 · see citing works
Dynamics and stability of legged locomotion in the horizontal plane: a test case using insects
Schmitt, J., Garcia, M., Razo, R. Q., et al. (2002) · Biological Cybernetics · doi:10.1007/s00422-001-0300-3 · Cited by 131 · see citing works
Ahn, A. N., & Full, R. J. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.3.379 · Cited by 128 · see citing works
Assessing sensory function in locomotor systems using neuro-mechanical simulations
Pearson, K. G., Ekeberg, Ö., & Büschges, A. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.08.007 · Cited by 127 · see citing works
Neuronal control of swimming behavior: Comparison of vertebrate and invertebrate model systems
Mullins, O. J., Hackett, J. T., Buchanan, J. T., & Friesen, W. O. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.11.001 · Cited by 105 · see citing works
The Critical Role of Locomotion Mechanics in Decoding Sensory Systems
Cowan, N. J., & Fortune, E. S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4198-06.2007 · Cited by 98 · see citing works
Impedance is modulated to meet accuracy demands during goal-directed arm movements
Selen, L. P. J., Beek, P. J., & van Dieën, J. H. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-0320-7 · Cited by 97 · see citing works
Iwasaki, T., & Zheng, M. (2006) · Biological Cybernetics · doi:10.1007/s00422-005-0047-3 · Cited by 97 · see citing works
McMillen, T., Williams, T. L., & Holmes, P. J. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000157 · Cited by 89 · see citing works
Self-citationAn elastic rod model for anguilliform swimming
McMillen, T., & Holmes, P. J. (2006) · Journal of Mathematical Biology · doi:10.1007/s00285-006-0036-8 · Cited by 87 · see citing works
Self-citationInsects running on elastic surfaces
Spence, A. J., Revzen, S., Seipel, J. E., et al. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.042515 · Cited by 86 · see citing works
Dynamics and stability of insect locomotion: a hexapedal model for horizontal plane motions
Seipel, J. E., Holmes, P. J., & Full, R. J. (2004) · Biological Cybernetics · doi:10.1007/s00422-004-0498-y · Cited by 85 · see citing works
Self-citationMechanisms underlying rhythmic locomotion: body–fluid interaction in undulatory swimming
Chen, J., Friesen, W. O., & Iwasaki, T. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.048751 · Cited by 80 · see citing works
Muscle mechanics and neuromuscular control
Hof, A. L. (2003) · Journal of Biomechanics · doi:10.1016/s0021-9290(03)00036-8 · Cited by 77 · see citing works
The biomechanics of sensory organs
Sane, S. P., & McHenry, M. J. (2009) · Integrative and Comparative Biology · doi:10.1093/icb/icp112 · Cited by 73 · see citing works
Beek, P. J., & Lewbel, A. (1995) · Scientific American · doi:10.1038/scientificamerican1195-92 · Cited by 69 · see citing works
The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal
Lin, H. T., & Trimmer, B. A. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.037796 · Cited by 68 · see citing works
Biomechanics — Structures and Systems
(1992) · doi:10.1093/oso/9780199632688.001.0001 · Cited by 68 · see citing works
Next-Generation Actuators Leading Breakthroughs
Higuchi, T., Suzumori, K., & Tadokoro, S. (2009) · Springer eBooks · doi:10.1007/978-1-84882-991-6 · Cited by 65 · see citing works
Formal analysis of resonance entrainment by central pattern generator
Futakata, Y., & Iwasaki, T. (2008) · Journal of Mathematical Biology · doi:10.1007/s00285-007-0151-1 · Cited by 63 · see citing works
Kukillaya, R. P., Proctor, J. L., & Holmes, P. J. (2009) · Chaos An Interdisciplinary Journal of Nonlinear Science · doi:10.1063/1.3141306 · Cited by 61 · see citing works
Self-citationReflexes and preflexes: on the role of sensory feedback on rhythmic patterns in insect locomotion
Proctor, J. L., & Holmes, P. J. (2010) · Biological Cybernetics · doi:10.1007/s00422-010-0383-9 · Cited by 61 · see citing works
Self-citationCouzin-Fuchs, E. (2010) · Frontiers in Neural Circuits · doi:10.3389/fncir.2010.00125 · Cited by 60 · see citing works
Sponberg, S., Spence, A. J., Mullens, C. H., et al. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0367 · Cited by 57 · see citing works
Anguilliform body dynamics: modelling the interaction between muscle activation and body curvature
Bowtell, G., & Williams, T. L. (1991) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1991.0123 · Cited by 55 · see citing works
Neuromechanics of Multifunctionality during Rejection in Aplysia californica
Ye, H., Morton, D. W., & Chiel, H. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3143-06.2006 · Cited by 54 · see citing works
Verdaasdonk, B. W., Koopman, H. F. J. M., & van der Helm, F. C. T. (2009) · Biological Cybernetics · doi:10.1007/s00422-009-0316-7 · Cited by 46 · see citing works
Bowtell, G., & Williams, T. L. (1994) · Journal of Mathematical Biology · doi:10.1007/bf00163025 · Cited by 39 · see citing works
A hexapedal jointed-leg model for insect locomotion in the horizontal plane
Kukillaya, R. P., & Holmes, P. J. (2007) · Biological Cybernetics · doi:10.1007/s00422-007-0180-2 · Cited by 38 · see citing works
Self-citationNext generation actuators leading breakthroughs
Higuchi, T. (2010) · Journal of Mechanical Science and Technology · doi:10.1007/s12206-009-1153-2 · Cited by 38 · see citing works
Shifts in a single muscle's control potential of body dynamics are determined by mechanical feedback
Sponberg, S., Libby, T., Mullens, C. H., et al. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0368 · Cited by 36 · see citing works
Proctor, J. L., Kukillaya, R. P., & Holmes, P. J. (2010) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2010.0134 · Cited by 35 · see citing works
Self-citationThree-dimensional Translational Dynamics and Stability of Multi-legged Runners
Seipel, J. E., & Holmes, P. J. (2006) · The International Journal of Robotics Research · doi:10.1177/0278364906069045 · Cited by 33 · see citing works
Self-citationA comparison of resonance tuning with positive versus negative sensory feedback
Williams, C. A., & DeWeerth, S. P. (2007) · Biological Cybernetics · doi:10.1007/s00422-007-0150-8 · Cited by 31 · see citing works
Steering by transient destabilization in piecewise-holonomic models of legged locomotion
Proctor, J. L., & Holmes, P. J. (2008) · Regular and Chaotic Dynamics · doi:10.1134/s1560354708040047 · Cited by 30 · see citing works
Self-citationKukillaya, R. P., & Holmes, P. J. (2009) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2009.07.036 · Cited by 26 · see citing works
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- Authors
- Tytell, E., Holmes, P., & Cohen, A.
- Affiliations
- Johns Hopkins University (US)
- Princeton University (US)
- University of Maryland, College Park (US)
- Corresponding author
- Tytell, ED
- ORCID
- Holmes, P
- Venue
- Current Opinion in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2011-10
- Volume
- 21
- Issue
- 5
- Pages
- 816-822
- ISSN
- 0959-4388 (ISSN-L)
- PMC
- PMC3183174
- OpenAlex
- W2074310014
- Semantic Scholar
- 6453ae0e0c4190f829a1e909e70cf4b5bc93cc29
- Cited by
- 135
- References
- 69
- Citations by year
- 2026: 7 · 2025: 3 · 2024: 15 · 2023: 12 · 2022: 19 · 2021: 12 · 2020: 11 · 2019: 9 · 2018: 13 · 2017: 5 · 2016: 5 · 2015: 8 · 2014: 6 · 2013: 5 · 2012: 5
- FWCI
- 0.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Current Opinion in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (MH62196, P50MH062196)
- National Institute of Neurological Disorders and Stroke (R01NS054271, F32NS054367)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Physical Sciences › Engineering › Biomedical Engineering › Robotic Locomotion and Control
- Life Sciences › Neuroscience › Cognitive Neuroscience › Embodied and Extended Cognition
- Keywords
- neuromechanics, neural circuits, muscle mechanics, body stiffness, leg stiffness, robustness to disturbances, sensory reflexes, neural control of movement, behavior
- MeSH terms
- Action Potentials, Animals, Biomechanical Phenomena, Humans, Models, Neurological, Neurons, Neurosciences
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