Skip to main content
SpringerLink
Log in

Deriving neural network controllers from neuro-biological data: implementation of a single-leg stick insect controller

  • Original Paper
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

This article presents modular recurrent neural network controllers for single legs of a biomimetic six-legged robot equipped with standard DC motors. Following arguments of Ekeberg et al. (Arthropod Struct Dev 33:287–300, 2004), completely decentralized and sensori-driven neuro-controllers were derived from neuro-biological data of stick-insects. Parameters of the controllers were either hand-tuned or optimized by an evolutionary algorithm. Employing identical controller structures, qualitatively similar behaviors were achieved for robot and for stick insect simulations. For a wide range of perturbing conditions, as for instance changing ground height or up- and downhill walking, swing as well as stance control were shown to be robust. Behavioral adaptations, like varying locomotion speeds, could be achieved by changes in neural parameters as well as by a mechanical coupling to the environment. To a large extent the simulated walking behavior matched biological data. For example, this was the case for body support force profiles and swing trajectories under varying ground heights. The results suggest that the single-leg controllers are suitable as modules for hexapod controllers, and they might therefore bridge morphological- and behavioral-based approaches to stick insect locomotion control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander RM (1989) Optimization and gaits in the locomotion of vertebrates. Physiol Rev 69: 1199–1227

    PubMed  CAS  Google Scholar 

  • Azevedo C, Espiau B, Amblard B, Assaiante C (2007) Bipedal locomotion: toward unified concepts in robotics and neuroscience. Biol Cybern 96: 209–228

    Article  PubMed  Google Scholar 

  • Bartling C, Schmitz J (2000) Reaction to disturbances of a walking leg during stance. J Exp Biol 203: 1211–1223

    PubMed  CAS  Google Scholar 

  • Bässler U (1983) Neural basis of elementary behavior in stick insects. Springer, Berlin

    Google Scholar 

  • Bässler U (1988) Functional principles of pattern generation for walking movements of stick insect forelegs: the role of the femoral chordotonal organ afferences. J Exp Biol 136: 125–147

    Google Scholar 

  • Bässler U (1993) The femur-tibia control system of stick insects a model system for the study of the neural basis of joint control. Brain Res Rev 18(2): 207–226

    Article  PubMed  Google Scholar 

  • Bässler U, Büschges A (1998) Pattern generation for stick insect walking movements—multisensory control of a locomotor program. Brain Res Rev 27: 65–88

    Article  PubMed  Google Scholar 

  • Beer RD (2006) Beyond control: the dynamics of brain-body-environment interaction in motor systems. In: Sternard D (eds) Progress in motor control V: a multidisciplinary perspective. Springer, Berlin, pp 7–24

    Google Scholar 

  • Beer RD, Quinn RD, Chiel HJ, Ritzmann RE (1997) Biologically inspired approaches to robotics—what can we learn from insects. Commun ACM 40(3): 31–38

    Article  Google Scholar 

  • Bekey GA (2005) Autonomous robots—from biological inspiration to implementation and control. MIT Press, Cambridge

    Google Scholar 

  • Biewener AA (2005) Biomechanical consequences of scaling. J Exp Biol 208: 1665–1676

    Article  PubMed  Google Scholar 

  • Blaesing B, Cruse H (2004) Stick insect locomotion in a complex environment: climbing over large gaps. J Exp Biol 207: 1273–1286

    Article  PubMed  Google Scholar 

  • Borgmann A, Scharstein H, Büschges A (2007) Intersegmental coordination: influence of a single walking leg on the neighboring segments in the stick insect walking system. J Neurophysiol 98: 1685–1696

    Article  PubMed  Google Scholar 

  • Borgmann A, Hooper SL, Büschges A (2009) Sensory feedback induced by front-leg stepping entrains the activity of central pattern generators in caudal segments of the stick insect walking system. J Neurosci 29(9): 2972–2983

    Article  PubMed  CAS  Google Scholar 

  • Brunn DE, Dean J (1994) Intersegmental and local interneurons in the metathorax of the stick insect carausius morosus that monitor middle leg position. J Neurophysiol 72(3): 1208–1219

    PubMed  CAS  Google Scholar 

  • Bucher D, Akay T, DiCaprio RA, Büschges A (2003) Interjoint coordination in the stick insect leg-control system: the role of positional signaling. J Neurophysiol 89: 1245–1255

    Article  PubMed  Google Scholar 

  • Büschges A (2005) Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. J Neurophysiol 93: 1127–1135

    Article  PubMed  Google Scholar 

  • Büschges A, Kittmann R, Schmitz J (1994) Identified nonspiking interneurons in leg reflexes and during walking in the stick insect. J Comp Physiol A 174: 685–700

    Article  Google Scholar 

  • Büschges A, Akay T, Gabriel JP, Schmidt J (2008) Organizing network action for locomotion: insights from studying insect walking. Brain Res Rev 57: 162–171

    Article  PubMed  Google Scholar 

  • Calvitti A, Beer RD (2000) Analysis of a distributed model of leg coordination i. Individual coordination mechanisms. Biol Cybern 82: 197–206

    Article  PubMed  CAS  Google Scholar 

  • Chiel HJ, Ting LH, Ekeberg O, Hartmann MJZ (2009) The brain in its body: Motor control and sensing in a biomechanical context. J Neurosci 29(41): 12807–12814

    Article  PubMed  CAS  Google Scholar 

  • Cruse H (1976) The function of the legs in the free walking stick insect, carausius morosus. J Comp Physiol A 112: 235–262

    Article  Google Scholar 

  • Cruse H (1980) A quantitative model of walking incorporating central and peripheral influences i. The control of the individual leg. Biol Cybern 37: 131–136

    Article  Google Scholar 

  • Cruse H (1990) What mechanisms coordinate leg movement in walking arthropods. Trends Neurosci 13: 15–21

    Article  PubMed  CAS  Google Scholar 

  • Cruse H, Bartling C (1995) Movement of joint angles in the legs of a walking insect, carausius morosus. J Insect Physiol 41(9): 761–771

    Article  Google Scholar 

  • Cruse H, Schmitz J, Braun U, Schweins A (1993) Control of body height in a stick insect walking on a treadwheel. J Exp Biol 181(1): 141–155

    Google Scholar 

  • Cruse H, Kühn S, Park S, Schmitz J (2004) Adaptive control for insect leg position: controller properties depend on substrate compliance. J Comp Physiol A 190(12): 983–991

    Article  CAS  Google Scholar 

  • Cruse H, Dürr V, Schmitz J (2007) Insect walking is based on a decentralized architecture revealing a simple and robust controller. Philos Trans R Soc A 365(1850): 221–250

    Article  Google Scholar 

  • Daun-Gruhn S (2010) A mathematical modeling study of inter-segmental coordination during stick insect walking. J Comput Neurosci, pp 1–24. http://dx.doi.org/10.1007/s10827-010-0254-3, online first

  • Dean J (1991) Effect of load on leg movement and step coordination of the stick insect carausius morosus. J Exp Biol 159: 449–471

    Google Scholar 

  • Dickinson MH, Farley CT, Full RJ, Koehl MAR, Kram R, Lehmann S (2000) How animals move: an integrative view. Science 288: 100–106

    Article  PubMed  CAS  Google Scholar 

  • Dürr V (2001) Stereotypic leg searching movements in the stick insect: kinematic analysis, behavioural context and simulation. J Exp Biol 204: 1589–1604

    PubMed  Google Scholar 

  • Dürr V (2005) Context-dependent changes in strength and efficacy of leg coordination mechanisms. J Exp Biol 208: 2253–2267

    Article  PubMed  Google Scholar 

  • Dürr V, Schmitz J, Cruse H (2004) Behaviour-based modelling of hexapod locomotion: linking biology and technical application. Arthropod Struct Dev 33: 237–250

    Article  PubMed  Google Scholar 

  • Ekeberg O, Blümel M, Büschges A (2004) Dynamic simulation of insect walking. Arthropod Struct Dev 33: 287–300

    Article  PubMed  Google Scholar 

  • Fischer H, Schmidt J, Haas R, Büschges A (2001) Pattern generation for walking and searching movements of a stick insect leg. i. Coordination of motor activity. J Neurophysiol 85: 341–353

    PubMed  CAS  Google Scholar 

  • Foth E, Graham D (1983) Influence of loading parallel to the body axis on the walking coordination of an insect—I. Ipsilateral effects. Biol Cybern 47(1): 17–23

    Google Scholar 

  • Frigon A, Rossignol S (2006) Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95(6): 607–627

    Article  PubMed  Google Scholar 

  • Full RJ, Blickhan R, Ting LH (1991) Leg design in hexapedal runners. J Exp Biol 158: 369–390

    PubMed  CAS  Google Scholar 

  • Gabriel JP, Büschges A (2007) Control of stepping velocity in a single insect leg during walking. Philos Trans R Soc A 365: 251–271

    Article  Google Scholar 

  • Gabriel JP, Scharstein H, Schmidt J, Büschges A (2003) Control of flexor motoneuron activity during single leg walking of the stick insect on an electronically controlled treadwheel. J Neurobiol 56: 237–251

    Article  PubMed  Google Scholar 

  • Ghazi-Zahedi KM (2008) Self-regulating neurons. A model for synaptic plasticity in artificial recurrent neural networks. PhD thesis, University of Osnabrück

  • Goslow GE, Reinking RM, Stuart DG (1973) The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141(1): 1–41

    Article  PubMed  Google Scholar 

  • Graham D (1972) A behavioural analysis of the temporal organization of walking movements in the 1st instar and adult stick insect Carausius morosus. J Comp Physiol 81: 23–52

    Article  Google Scholar 

  • Graham D (1983) Insects are both impeded and propelled by their legs during walking. J Exp Biol 104: 129–137

    Google Scholar 

  • Graham D (1985) Pattern and control of walking in insects. Adv Insect Physiol 18: 31–140

    Article  Google Scholar 

  • Graham D, Cruse H (1981) Coordinated walking of stick insects on a mercury surface. J Exp Biol 92: 229–241

    Google Scholar 

  • Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52(5): 751–766

    Article  PubMed  CAS  Google Scholar 

  • Gruhn M, von Uckermann G, Westmark S, Wosnitza A, Büschges A, Borgmann A (2009) Control of stepping velocity in the stick insect carausius morosus. J Neurophysiol 102: 1180–1192

    Article  PubMed  Google Scholar 

  • Guschlbauer C, Scharstein H, Büschges A, (2007) The extensor tibiae muscle of the stick insect: biomechanical properties of an insect walking muscle. J Exp Biol 210:1092–1108

    Article  PubMed  Google Scholar 

  • Halbertsma J (1983) The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. Acta Physiol Scand Suppl 521: 1–75

    PubMed  CAS  Google Scholar 

  • Hatsopoulos NG (1996) Coupling the neural and physical dynamics in rhythmic movements. Neural Comput 8: 567–581

    Article  PubMed  CAS  Google Scholar 

  • Hess D, Büschges A (1997) Sensorimotor pathways involved in interjoint reflex action of an insect leg. J Neurobiol 33(7): 891–913

    Article  PubMed  CAS  Google Scholar 

  • Hooper SL, Guschlbauer C, von Uckermann G, Büschges A (2007) Slow temporal filtering may largely explain the transformation of stick insect (carausius morosus) extensor motor neuron activity into muscle movement. J Neurophysiol 98: 1718–1732

    Article  PubMed  Google Scholar 

  • Hooper SL, Guschlbauer C, Blümel M, Rosenbaum P, Gruhn M, Akay T, Büschges A (2009) Neural control of unloaded leg posture and of leg swing in stick insect cockroach, and mouse differs from that in larger animals. J Neurosci 29(13): 4109–4119

    Article  PubMed  CAS  Google Scholar 

  • Hülse M, Pasemann F (2006) Modular design of irreducible systems. In: Nolfi S, et al (eds) From animals to Animats 9 (SAB 2006), LNAI, vol 4095. Springer, Berlin. pp 534–545

  • Hülse M, Wischmann S, Pasemann F (2004) Structure and function of evolved neuro-controllers for autonomous robots. Connect Sci 16(4): 249–266

    Article  Google Scholar 

  • Hülse M, Wischmann S, von Twickel A, Manoonpong P, Pasemann F (2007) Dynamical systems in the sensorimotor loop—on the interrelation between internal and external mechanisms of evolved robot behavior. In: Lungarella M, et al (eds) 50 years of artificial intelligence, LNAI, vol 4850. Springer, Berlin, pp 186–195

  • Ijspeert A, Crespi A, Ryczko D, Cabelguen JM (2007) From swimming to walking with a salamander robot driven by a spinal cord model. Science 315(5817): 1416–1420

    Article  PubMed  CAS  Google Scholar 

  • Ijspeert AJ (2008) Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21(4): 642–653

    Article  PubMed  Google Scholar 

  • Kindermann T (2002) Behavior and adaptability of a six-legged walking system with highly distributed control. Adapt Behav 9(1): 16–41

    Article  Google Scholar 

  • Komsuoglu H, Sohn K, Full RJ, Koditschek DE (2009) A physical model for dynamical arthropod running on level ground. In: Khatib O, et al (eds) Experimental robotics—the eleventh international symposium, Springer, pp 303–317

  • Lévy J, Cruse H (2008) Controlling a system with redundant degrees of freedom: II. Solution of the force distribution problem without a body model. J Comp Physiol A 194(8): 735–750

    Article  Google Scholar 

  • Lewinger WA, Rutter BL, Blümel M, Büschges A, Quinn RD (2006) Sensory coupled action switching modules (SCASM) generate robust, adaptive stepping in legged robots. In: Proceedings of the 9th international conference on climbing and walking robots (CLAWAR 2006), Brussels

  • Linder CR (2005) Embodiment in two dimensions. In: Proceedings of the 7th international conference on climbing and walking robots, 2004

  • Ludwar BC, Göritz ML, Schmidt J (2005) Intersegmental coordination of walking movements in stick insects. J Neurophysiol 93: 1255–1265

    Article  PubMed  Google Scholar 

  • Manoonpong P, Pasemann F, Wörgötter F (2008) Sensor-driven neural control for omnidirectional locomotion and versatile reactive behaviors of walking machines. Robot Auton Syst 56(3): 265–288

    Article  Google Scholar 

  • Maufroy C, Kimura H, Takase K (2008) Towards a general neural controller for quadrupedal locomotion. Neural Netw 21: 667–681

    Article  PubMed  Google Scholar 

  • Negrello M, Hülse M, Pasemann F (2008) Adaptive neurodynamics. In: Yang A, Shan Y (eds) Applications of complex adaptive systems. Idea Group, Hershey, pp 85–111

    Google Scholar 

  • Nolfi S, Floreano D (2000) Evolutionary robotics: the biology, intelligence, and technology of self-organizing machines. MIT Press, Cambridge

    Google Scholar 

  • Orlovsky G, Deliagina T, Grillner S (1999) Neuronal control of locomotion. Oxford University Press, Oxford

    Google Scholar 

  • Pasemann F (1995) Characterization of periodic attractors in neural ring networks. Neural Netw 8: 421–429

    Article  Google Scholar 

  • Pasemann F, Steinmetz U, Hülse M, Lara B (2001) Robot control and the evolution of modular neurodynamics. Theory Biosci 120: 311–326

    Google Scholar 

  • Pearson K, Iles J (1973) Nervous mechanisms underlying intersegmental co-ordination of leg movements during walking in the cockroach. J Exp Biol 58: 725–744

    Google Scholar 

  • Pearson K, Ekeberg O, Büschges A (2006) Assessing sensory function in locomotor systems using neuro-mechanical simulations. Trends Neurosci 29(11): 625–631

    Article  PubMed  CAS  Google Scholar 

  • Pfeifer R, Bongard J (2006) How the body shapes the way we think—a new view of intelligence. MIT Press, Cambridge

    Google Scholar 

  • Revzen S, Koditschek DE, Full RJ (2009) Towards testable neuromechanical control architectures for running. In: Sternad D (ed) Progress in motor control—a multidisciplinary perspective, Advances In Experimental Medicine And Biology, vol 629. Springer, Berlin, pp 25–56

  • Ritzmann RE, Büschges A (2007) Insect walking: from reduced preparations to natural terrain. In: North G, Greenspan RJ (eds) Invertebrate neurobiology. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 229–250

    Google Scholar 

  • Rutter BL, Lewinger WA, Blümel M, Büschges A, Quinn RD (2007) Simple muscle models regularize motion in a robotic leg with neurally-based step generation. In: 2007 IEEE international conference on robotics and automation, Roma, pp 630–635

  • Schilling M, Cruse H, Arena P (2007) Hexapod walking: an expansion to walknet dealing with leg amputations and force oscillations. Biol Cybern 96(3): 323–340

    Article  PubMed  Google Scholar 

  • Schumm M, Cruse H (2006) Control of swing movement: influences of differently shaped substrate. J Comp Physiol A 192(10): 1147–1164

    Article  Google Scholar 

  • Smith R (2009) Open dynamics engine. http://www.ode.org, last visited: 18/11/2009

  • von Twickel A, Pasemann F (2007) Reflex-oscillations in evolved single leg neurocontrollers for walking machines. Nat Comput 6(3): 311–337

    Article  Google Scholar 

  • von Uckermann G, Büschges A (2009) Premotor interneurons in the local control of stepping motor output for the stick insect single middle leg. J Neurophysiol 102: 1956–1975

    Article  Google Scholar 

  • Webb B (2009) Animals versus animats: or why not model the real iguana. Adapt Behav 17(4): 269–286

    Article  Google Scholar 

  • Wendler G (1964) Laufen und stehen der stabheuschrecke carausius morosus: sinnesborstenfelder in den beingelenken als glieder von regelkreisen. Z vgl Physiol 48: 198–250

    Article  Google Scholar 

  • Wolf H, Büschges A (1995) Nonspiking local interneurons in insect leg motor control. ii. role of nonspiking local interneurons in the control of leg swing during walking. J Neurophysiol 73: 1861–1875

    PubMed  CAS  Google Scholar 

  • Yakovenko S, Gritsenko V, Prochazka A (2004) Contribution of stretch reflexes to locomotor control: a modeling study. Biol Cybern 90(2): 146–155

    Article  PubMed  CAS  Google Scholar 

  • Yakovenko S, McCrea D, Stecina K, Prochazka A (2005) Control of locomotor cycle durations. J Neurophysiol 94: 1057–1065

    Article  PubMed  CAS  Google Scholar 

  • Zahedi K, von Twickel A, Pasemann F (2008) Yars: a physical 3d simulator for evolving controllers for real robots. In: Carpin S, et al (eds) Simulation, modeling and programming for autonomous robots (SIMPAR 2008), LNAI, vol 5325. Springer, pp 75–86

Download references

Author information

Authors and Affiliations

  1. Department of Neurocybernetics, Institute of Cognitive Science, University of Osnabrück, 49069, Osnabrück, Germany

    Arndt von Twickel & Frank Pasemann

  2. Institute for Advanced Study, Wallotstraße 19, 14193, Berlin, Germany

    Arndt von Twickel & Frank Pasemann

  3. Department of Animal Physiology, Zoological Institute, University of Cologne, 50674, Cologne, Germany

    Ansgar Büschges

Authors
  1. Arndt von Twickel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ansgar Büschges
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frank Pasemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arndt von Twickel.

Electronic Supplementary Material

The Below is the Electronic Supplementary Material.

ESM 1 (PDF 327 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

von Twickel, A., Büschges, A. & Pasemann, F. Deriving neural network controllers from neuro-biological data: implementation of a single-leg stick insect controller. Biol Cybern 104, 95–119 (2011). https://doi.org/10.1007/s00422-011-0422-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-011-0422-1

Keywords

Search

Navigation