An energy landscape approach to locomotor transitions in complex 3D terrain

Significance Effective locomotion in nature happens by transitioning across multiple modes (e.g., walk, run, climb). Using laboratory experiments on a model system, we demonstrate that an energy landscape approach helps understand how multipathway transitions across locomotor modes in complex 3D terrain statistically emerge from physical interaction. Animals’ and robots’ locomotor modes are attracted to basins of a potential energy landscape. They can use kinetic energy fluctuation from oscillatory self-propulsion to cross potential energy barriers, escaping from one basin and reaching another to make locomotor transitions. Our first-principle energy landscape approach is the beginning of a statistical physics theory of locomotor transitions in complex terrain. It will help understand and predict how animals, and how robots should, move through the real world. Effective locomotion in nature happens by transitioning across multiple modes (e.g., walk, run, climb). Despite this, far more mechanistic understanding of terrestrial locomotion has been on how to generate and stabilize around near–steady-state movement in a single mode. We still know little about how locomotor transitions emerge from physical interaction with complex terrain. Consequently, robots largely rely on geometric maps to avoid obstacles, not traverse them. Recent studies revealed that locomotor transitions in complex three-dimensional (3D) terrain occur probabilistically via multiple pathways. Here, we show that an energy landscape approach elucidates the underlying physical principles. We discovered that locomotor transitions of animals and robots self-propelled through complex 3D terrain correspond to barrier-crossing transitions on a potential energy landscape. Locomotor modes are attracted to landscape basins separated by potential energy barriers. Kinetic energy fluctuation from oscillatory self-propulsion helps the system stochastically escape from one basin and reach another to make transitions. Escape is more likely toward lower barrier direction. These principles are surprisingly similar to those of near-equilibrium, microscopic systems. Analogous to free-energy landscapes for multipathway protein folding transitions, our energy landscape approach from first principles is the beginning of a statistical physics theory of multipathway locomotor transitions in complex terrain. This will not only help understand how the organization of animal behavior emerges from multiscale interactions between their neural and mechanical systems and the physical environment, but also guide robot design, control, and planning over the large, intractable locomotor-terrain parameter space to generate robust locomotor transitions through the real world.

[1]  H. Cruse,et al.  Stick insect locomotion in a complex environment: climbing over large gaps , 2004, Journal of Experimental Biology.

[2]  J. Onuchic,et al.  Theory of Protein Folding This Review Comes from a Themed Issue on Folding and Binding Edited Basic Concepts Perfect Funnel Landscapes and Common Features of Folding Mechanisms , 2022 .

[3]  R. Full,et al.  Cockroaches use diverse strategies to self-right on the ground , 2019, Journal of Experimental Biology.

[4]  Steven Vogel,et al.  Twist-to-Bend Ratios and Cross-Sectional Shapes of Petioles and Stems , 1992 .

[5]  W. H. Warren,et al.  Why change gaits? Dynamics of the walk-run transition. , 1995, Journal of experimental psychology. Human perception and performance.

[6]  Sebastian Thrun,et al.  Toward robotic cars , 2010, CACM.

[7]  K. Dill,et al.  The Protein-Folding Problem, 50 Years On , 2012, Science.

[8]  Arthur D Kuo,et al.  The six determinants of gait and the inverted pendulum analogy: A dynamic walking perspective. , 2007, Human movement science.

[9]  Auke Jan Ijspeert,et al.  Central pattern generators for locomotion control in animals and robots: A review , 2008, Neural Networks.

[10]  J. Gibson The Ecological Approach to Visual Perception , 1979 .

[11]  G. Swaminathan Robot Motion Planning , 2006 .

[12]  Metin Sitti,et al.  Small-scale soft-bodied robot with multimodal locomotion , 2018, Nature.

[13]  Brian R. Tietz,et al.  Deciding Which Way to Go: How Do Insects Alter Movements to Negotiate Barriers? , 2012, Front. Neurosci..

[14]  Jasmine A. Nirody,et al.  The mechanics of slithering locomotion , 2009, Proceedings of the National Academy of Sciences.

[15]  W. Davis The Ecological Approach to Visual Perception , 2012 .

[16]  H. Baier,et al.  Deconstructing Hunting Behavior Reveals a Tightly Coupled Stimulus-Response Loop , 2019, Current Biology.

[17]  Gordon J. Berman,et al.  Measuring behavior across scales , 2017, BMC Biology.

[18]  A. Biewener,et al.  Negotiating obstacles: running kinematics of the lizard Sceloporus malachiticus , 2006 .

[19]  C. Wilmers,et al.  Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice. , 2019, Ecology letters.

[20]  Vincent A. Voelz,et al.  Slow unfolded-state structuring in Acyl-CoA binding protein folding revealed by simulation and experiment. , 2012, Journal of the American Chemical Society.

[21]  W. Bialek,et al.  Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans , 2011, Proceedings of the National Academy of Sciences.

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

[23]  Chen Li,et al.  Body-terrain interaction affects large bump traversal of insects and legged robots , 2018, Bioinspiration & biomimetics.

[24]  KHLow,et al.  Perspectives on biologically inspired hybrid and multi-modal locomotion , 2015 .

[25]  K. Niklas The elastic moduli and mechanics of Populus tremuloides (Salicaceae) petioles in bending and torsion , 1991 .

[26]  Gordon J. Berman,et al.  Optogenetic dissection of descending behavioral control in Drosophila , 2017, bioRxiv.

[27]  Chen Li,et al.  Multi-functional foot use during running in the zebra-tailed lizard (Callisaurus draconoides) , 2012, Journal of Experimental Biology.

[28]  M. V. Folegatti,et al.  Estimation of leaf area for greenhouse cucumber by linear measurements under salinity and grafting , 2005 .

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

[30]  D. Bramble,et al.  Endurance running and the evolution of Homo , 2004, Nature.

[31]  Andrew M. Mountcastle,et al.  BEEtag: A Low-Cost, Image-Based Tracking System for the Study of Animal Behavior and Locomotion , 2015, bioRxiv.

[32]  Greg J. Stephens,et al.  Dimensionality and Dynamics in the Behavior of C. elegans , 2007, PLoS Comput. Biol..

[33]  Benjamin L. de Bivort,et al.  Ethology as a physical science , 2018, Nature Physics.

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

[35]  H. Benjamin Brown,et al.  c ○ 2001 Kluwer Academic Publishers. Manufactured in The Netherlands. RHex: A Biologically Inspired Hexapod Runner ∗ , 2022 .

[36]  Chen Li,et al.  A Terradynamics of Legged Locomotion on Granular Media , 2013, Science.

[37]  R J Full,et al.  Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain , 2008, Journal of Experimental Biology.

[38]  S C Burgess,et al.  Multi-modal locomotion: from animal to application , 2013, Bioinspiration & biomimetics.

[39]  Michael F. Ashby,et al.  Structure and mechanics of the iris leaf , 1988 .

[40]  Howie Choset,et al.  A review on locomotion robophysics: the study of movement at the intersection of robotics, soft matter and dynamical systems , 2016, Reports on progress in physics. Physical Society.

[41]  A. R. Ennos The Mechanics of the Flower Stem of the Sedge Carex acutiformis , 1993 .

[42]  A. Garrod Animal Locomotion , 1874, Nature.

[43]  Reinhard Blickhan,et al.  Compliant leg behaviour explains basic dynamics of walking and running , 2006, Proceedings of the Royal Society B: Biological Sciences.

[44]  Tyson L Hedrick,et al.  Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems , 2008, Bioinspiration & biomimetics.

[45]  Julius Jellinek,et al.  Energy Landscapes: With Applications to Clusters, Biomolecules and Glasses , 2005 .

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

[47]  R. Full,et al.  Three-dimensional kinematics and limb kinetic energy of running cockroaches. , 1997, The Journal of experimental biology.

[48]  J. L. de la Pompa,et al.  A novel source of arterial valve cells linked to bicuspid aortic valve without raphe in mice , 2018, eLife.

[49]  Chen Li,et al.  A template model reveals self-righting mechanism of a winged robot , 2020 .

[50]  R. McNeill Alexander,et al.  Principles of Animal Locomotion , 2002 .

[51]  Katie Byl,et al.  Metastable Walking Machines , 2009, Int. J. Robotics Res..

[52]  三嶋 博之 The theory of affordances , 2008 .

[53]  Sergio A. Lambertucci,et al.  Energy Landscapes Shape Animal Movement Ecology , 2013, The American Naturalist.

[54]  R. Emery,et al.  Uncoupling light quality from light irradiance effects in Helianthus annuus shoots: putative roles for plant hormones in leaf and internode growth. , 2007, Journal of experimental botany.

[55]  J. A. Scott Kelso,et al.  Multistability and metastability: understanding dynamic coordination in the brain , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  J. Onuchic,et al.  DIFFUSIVE DYNAMICS OF THE REACTION COORDINATE FOR PROTEIN FOLDING FUNNELS , 1996, cond-mat/9601091.

[57]  Andrew A Biewener,et al.  Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control , 2007, Journal of Experimental Biology.

[58]  Monica A. Daley,et al.  Don't break a leg: running birds from quail to ostrich prioritise leg safety and economy on uneven terrain , 2014, Journal of Experimental Biology.

[59]  Daniel E. Koditschek,et al.  Examples of Gibsonian Affordances in Legged Robotics Research Using an Empirical, Generative Framework , 2020, Frontiers in Neurorobotics.

[60]  P. Holmes,et al.  Intersegmental coupling and recovery from perturbations in freely running cockroaches , 2015, Journal of Experimental Biology.

[61]  Daniel E. Koditschek,et al.  Sequential Composition of Dynamically Dexterous Robot Behaviors , 1999, Int. J. Robotics Res..

[62]  E. Revilla,et al.  A movement ecology paradigm for unifying organismal movement research , 2008, Proceedings of the National Academy of Sciences.

[63]  Erico Guizzo,et al.  The hard lessons of DARPA's robotics challenge [News] , 2015 .

[64]  Chen Li,et al.  Terradynamically streamlined shapes in animals and robots enhance traversability through densely cluttered terrain , 2015, Bioinspiration & biomimetics.

[65]  E. Esmaili,et al.  Bending, twisting and flapping leaf upon raindrop impact , 2018, Bioinspiration & biomimetics.

[66]  Robert J. Full,et al.  Instantaneous kinematic phase reflects neuromechanical response to lateral perturbations of running cockroaches , 2013, Biological Cybernetics.

[67]  Duncan W. Haldane,et al.  Integrated Manufacture of Exoskeletons and Sensing Structures for Folded Millirobots , 2015 .

[68]  K. Dill,et al.  The protein folding problem. , 1993, Annual review of biophysics.

[69]  Chen Li,et al.  Body shape helps legged robots climb and turn in complex 3-D terrains , 2017 .

[70]  Ryan P. Adams,et al.  Mapping Sub-Second Structure in Mouse Behavior , 2015, Neuron.

[71]  G. E. Gale,et al.  Laboratory studies of the dynamic behaviour of grass, straw and polystyrene tube during high-speed cutting , 1991 .

[72]  Chen Li,et al.  Randomness in appendage oscillations helps a robot self-right , 2019 .

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

[74]  S. A. Etnier Twisting and Bending of Biological Beams: Distribution of Biological Beams in a Stiffness Mechanospace , 2003, The Biological Bulletin.

[75]  KasabovNikola,et al.  2008 Special issue , 2008 .

[76]  Kurt Wiesenfeld,et al.  A robot made of robots: Emergent transport and control of a smarticle ensemble , 2019, Science Robotics.

[77]  Joshua W. Shaevitz,et al.  Predictability and hierarchy in Drosophila behavior , 2016, Proceedings of the National Academy of Sciences.

[78]  P. Wolynes,et al.  Intermediates and barrier crossing in a random energy model , 1989 .

[79]  Sunghwan Jung,et al.  How wind drives the correlation between leaf shape and mechanical properties , 2018, Scientific Reports.