A systems approach to animal motor behavior reveals concepts that can be useful for the pragmatic design of walking machines. This is because the relation of animal behavior to its underlying nervous control algorithms bears many parallels to the relation of machine function to electronic control. Here, three major neuroethological concepts of motor behavior are described in terms of a conceptual framework based on artificial neural networks (ANN). Central patterns of activity and postural reflexes are both interpreted as a result of feedback loops, with the distinction of loops via an internal model from loops via the physical environment (body, external world). This view allows continuous transitions between predictive (centrally driven) and reactive (reflex driven) motor systems. Motor primitives, behavioral modules that are elicited by distinct commands, are also considered. ANNs capture these three major concepts in terms of a formal description, in which the interactions and mutual interdependences of the various output parameters are comprised by the weight matrix of the net. Based upon behavioral observations of insect walking, we further demonstrate how a decentralized network of separate modules, each one described by an ANN, can account for adaptive behavior. Complex coordination patterns of several manipulators are controlled by imposing simple interaction rules between limbs, and by exploiting the interaction of the body with its physical environment. Finally, we discuss the technical use of leg-like active tactile sensors for obstacle detection, and we show how specific design of such active sensors may increase efficiency of walking on rough terrain. Applied to active sensors, an example of parallel, self-organizing forward models on the basis of extended Kohonen maps is presented to emphasize the potential of adaptive forward models in motor control.
Get full access to this article
View all access options for this article.
References
1.
Akay, T., Bässler, U., Gerharz, P., and Büschges, A. 2001. The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint . Journal of Neurophysiology85: 594-604 .
2.
Bässler, U. 1983. Neural Basis of Elementary Behavior in Stick Insects, Springer, Berlin .
3.
Bässler, U., and Büschges, A. 1998. Pattern generation for stick insect walking movements—multisensory control of a locomotor program . Brain Research Reviews27: 65-88 .
4.
Berns, K., Cordes, S., and Ilg, W. 1994. Adaptive, neural control architecture for the walking machine Lauron . In Proceedings of the IEEE/RSJ International Conference on Intelligent Robots and Systems, München, Germany, 1172-1177 .
5.
Bizzi, E., Mussa-Ivaldi, F. A., and Giszter, S. F. 1991. Computations underlying the execution of movement: a biological perspective . Science253: 287-291 .
6.
Bizzi, E., Tresch, M. C., Saltiel, P., and d'Avella, A. 2000. New perspectives on spinal motor systems . Nature Reviews Neuroscience1: 101-108 .
7.
Bowerman, R.F. 1975. The control of walking in the scorpion. I. Leg movements during normal walking . Journal of Comparative Physiology100: 183-196 .
8.
Brooks, R. A. 1989. A robot that walks: Emergent behaviors from a carefully evolved network . Neural Computation1: 253-262 .
9.
Brooks, R. A. 1991. Intelligence without reason. In IJCAI-91, Sydney, Australia , 569-595.
10.
Büschges, A., Kittmann, R., and Schmitz, J. 1994. Identified nonspiking interneurons in leg reflexes and during walking in the stick insect . Journal of Comparative Physiology A174: 685-700 .
11.
Camhi, J. M., and Johnson, E. N. 1999. High-frequency steering maneuvers mediated by tactile cues: antennal wall-following in the cockroach . Journal of Experimental Biology202: 631-643 .
12.
Clarac, F. 1982. Decapod crustacean leg coordination during walking. In Herreid, C. F., and Fourtner, C. R., eds, Locomotion and Energetics in Arthropods, Plenum Press, New York , 31-71.
13.
Cruse, H. 1976. The control of body position in the stick insect (Carausius morosus), when walking over uneven surfaces . Biological Cybernetics24: 25-33 .
14.
Cruse, H. 1979. The control of the anterior extreme position of the hindleg of a walking insect , Carausius morosus. Physiological Entomology4: 121-124 .
15.
Cruse, H. 1990. What mechanisms coordinate leg movement in walking arthropods? Trends in Neurosciences13: 15-21 .
16.
Cruse, H. 2002. The functional sense of central oscillations in walking . Biological Cybernetics86: 271-280 .
17.
Cruse, H., and Bartling, C. 1995. Movement of joint angles in the legs of a walking insect , Carausius morosus. Journal of Insect Physiology41: 761-771 .
18.
Cruse, H., Bartling, C., Dreifert, M., Schmitz, J., Brunn, D. E., Dean, J., and Kindermann, T. 1995a. Walking: a complex behavior controlled by simple networks . Adaptive Behavior3: 385-418 .
19.
Cruse, H., Bartling, C., and Kindermann, T. 1995b. High-pass filtered positive feedback for decentralized control of cooperation. In Moran, F., Moreno, A., Merelo, J. J., and Chacon, P., eds, Advances in Artificial Life, Springer, Berlin , 668-678.
20.
Cruse, H., and Epstein, S. 1982. Peripheral influences on the movement of the legs in a walking insect Carausius morosus. Journal of Experimental Biology101: 161-170 .
21.
Cruse, H., Kindermann, T., Schumm, M., Dean, J., and Schmitz, J. 1998. Walknet—A biologically inspired network to control six-legged walking . Neural Networks11: 1435-1447 .
22.
Cruse, H., and Knauth, A. 1989. Coupling mechanisms between the contralateral legs of a walking insect (Carausius morosus) . Journal of Experimental Biology144: 199-213 .
23.
Cruse, H., and Müller, U. 1986. Two coupling mechanisms which determine the coordination of ipsilateral legs in the walking crayfish . Journal of Experimental Biology121: 349-369 .
24.
Cruse, H., Schmitz, J., Braun, U., and Schweins, A. 1993. Control of body height in a stick insect walking on a tread-wheel . Journal of Experimental Biology181: 141-155 .
25.
Cruse, H., and Schwarze, W. 1988. Mechanisms of coupling between the ipsilateral legs of a walking insect (Carausius morosus) . Journal of Experimental Biology138: 455-469 .
26.
Cuénot, L. 1921. Regeneration de pattes á la place d'antennes sectionnées chez un Phasme . Comptes Rendus de l'Académie des Sciences de Paris172: 949-952 .
27.
Dean, J., and Wendler, G. 1983. Stick insect locomotion on a walking wheel: interleg coordination of leg position . Journal of Experimental Biology103: 75-94 .
28.
Delcomyn, F. 1980. Neural basis of rhythmic behavior in animals . Science210: 492-498 .
29.
Delcomyn, F. 1987. Motor activity during searching and walking movements of cockroach legs . Journal of Experimental Biology133: 111-120 .
30.
Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R., Kram, R., and Lehman, S. 2000. How Animals Move: An Integrative View . Science288: 100-106 .
31.
Dürr, V. 2000. Grasping movements in an insect: Effects of tactile cues and step cycle phase . European Journal of Neuroscience12(Suppl. 11): 150 .
32.
Dürr, V. 2001. Stereotypic leg searching-movements in the stick insect: Kinematic analysis, behavioral context and simulation . Journal of Experimental Biology204: 1589-1604 .
33.
Dürr, V., König, Y., and Kittmann, R. 2001. The antennal motor system of the stick insect Carausius morosus: Anatomy and antennal movement pattern during walking . Journal of Comparative Physiology A187: 131-144 .
34.
Dürr, V., and Krause, A. 2002. Design of a biomimetic active tactile sensor for legged locomotion . In Bidaud, P., and Ben Amar, F., eds, Proc. 5th Int. Conf. on Climbing and Walking Robots, CLAWAR 2002, Paris, France. Professional Engineering Publishing, London, 255-262 .
35.
Edwards, D. H., Heitler, W. J., and Krasne, F. B. 1999. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish . Trends in Neurosciences22: 153-161 .
36.
Ekeberg, Ö., and Grillner, S. 1999. Simulations of the neuromuscular control in lamprey swimming . Philosophical Transactions of the Royal Society of London B354: 894-902 .
37.
Ekeberg, Ö., Lansner, A., and Grillner, S. 1995. The neural control of fish swimming studied through numerical simulation . Adaptive Behavior3: 363-384 .
38.
Espenschied, K. S., Quinn, R. D., Beer, R. D., and Chiel, H. J. 1996. Biologically based distributed control and local reflexes improve rough terrain locomotion in a hexapod robot . Robotics and Autonomous Systems18: 59-64 .
39.
Espenschied, K. S., Quinn, R. D., Chiel, H. J., and Beer, R. D. 1993. Leg coordination mechanisms in stick insect applied to hexapod robot locomotion . Adaptive Behavior1: 455-468 .
40.
Evoy, W., and Fourtner, C. R. 1973. Crustacean walking. In Stein, R. B., Pearson, K. G., Smith, R. S., and Redford, J. B., eds, Control of Posture and Locomotion, Plenum Press, New York , 477-493.
41.
Fischer, H., Schmidt, J., Haas, R., and Büschges, A. 2001. Pattern generation for walking and searching movements of a stick insect leg. I. Coordination of motor activity . Journal of Neurophysiology85: 341-353 .
42.
Frik, M., and Amendt, O. 1995. Neural control of a walking robot in variable terrain. In IFTOMM, Mailand, Italy , 2297-2301.
43.
Frik, M., Guddat, M., Karatas, M., and Losch, D. C. 1999. A novel approach to autonomous control of walking machines . In Proc. 2nd Int. Conf. on Climbing and Walking Robots, CLAWAR 99, Portsmouth, UK. Professional Engineering Publishing, London, 333-342 .
44.
Giszter, S. F., Loeb, E., Mussa-Ivaldi, F. A., and Bizzi, E. 2000. Repeatable spatial maps of a few force and joint torque patterns by microstimulation applied throughout the lumbar spinal cord of the spinal frog . Human Movement Science19: 597-626 .
45.
Giszter, S. F., Mussa-Ivaldi, F. A., and Bizzi, E. 1993. Convergent force fields in the frog's spinal cord . Journal of Neuroscience13: 467-491 .
46.
Graham, D. 1985. Pattern and control of walking in insects . Advances in Insect Physiology18: 31-140 .
47.
Grillner, S., Deliagina, T. G., Ekeberg, Ö., El Manira, A., Hill, R. H., Lansner, A., Orlovsky, G. N., and Wallén, P. 1995. Neural networks that co-ordinate locomotion and body orientation in lamprey . Trends in Neurosciences18: 270-279 .
48.
Harris, C. M., and Wolpert, D. M. 1998. Signal-dependent noise determines motor planning . Nature394: 780-784 .
49.
Haruno, M., Wolpert, D. M., and Kawato, M. 1999. Multiple paired forward-inverse models for human motor learning and control . Advances in Neural Information Processing Systems11: 31-37 .
50.
Hedwig, B. 1996. A descending brain neuron elicits stridulation in the cricket Gryllus bimaculatus (de Geer) . Naturwissenschaften83: 428-429 .
51.
Hedwig, B. 2001. Singing and hearing: Neuronal mechanisms of acoustic communication in Orthopterans . Zoology103: 140-149 .
52.
Honegger, H.-W. 1981. A preliminary note on a new optomotor response in crickets: Antennal tracking of moving targets . Journal of Comparative Physiology A142: 419-421 .
53.
Kaneko, M., Kanayma, N., and Tsuji, T. 1998. Active antenna for contact sensing . IEEE Transactions on Robotics and Automation14: 278-291 .
54.
Kindermann, T., and Cruse, H. 2002. MMC—A new numerical approach to the kinematics of complex manipulators . Mechanism and Machine Theory37: 375-394 .
55.
Linder, C. R. 2002. Self-organization in a simple task of motor control . In Proc. 7th Int. Conf. on the Simulation of Adaptive Behavior. From Animals to Animats7: 185-194 .
56.
Marder, E., and Bucher, D. 2001. Central pattern generators and the control of rhythmic movements . Current Biology11: R986-R996 .
57.
Miall, R. C., Weir, D. J., Wolpert, D. M., and Stein, J. F. 1993. Is the cerebellum a Smith predictor? Journal of Motor Behavior25: 203-216 .
58.
Minsky, M. 1985. The Society of Mind, Simon and Schuster, New York .
59.
Mussa-Ivaldi, F. A., Giszter, S. F., and Bizzi, E. 1994. Linear combinations of primitives in vertebrate motor control . Proceedings of the National Academy of Science USA91: 7534-7538 .
60.
Müller-Wilm, U., Dean, J., Cruse, H., Weidemann, H. J., Eltze, J., and Pfeiffer, F. 1992. Kinematic model of stick insect as an example of a 6-legged walking system . Adaptive Behavior1: 155-169 .
61.
Orlovsky, G. N., Deliagina, T. G., and Grillner, S. 1999. Neuronal Control of Locomotion. From Mollusk to Man, Oxford University Press, Oxford .
62.
Pearson, K. G., and Franklin, R. 1984. Characteristics of leg movements and patterns of coordination in locusts walking on rough terrain . International Journal of Robotics Research3: 101-112 .
63.
Pelletier, Y., and McLeod, C. D. 1994. Obstacle perception by insect antennae during terrestrial locomotion . Physiological Entomology19: 360-362 .
64.
Pfeiffer, F., Eltze, J., and Weidemann, H. J. 1995. Six-legged technical walking considering biological principles . Robotics and Autonomous Systems14: 223-232 .
65.
Pfeiffer, F., Weidemann, H. J., and Eltze, J. 1994. The TUM Walking Machine. Nguyen, and R. Lumial, eds. Intelligent Automation and Soft Computing. Trends in Research, Development and Applications, TSI Press, Albuquerque, NM , Vol. 2, 167-174.
66.
Reingold, S.C., and Camhi, J.M. 1977. A quantitative analysis of rhythmic leg movements during three different behaviors in the cockroach, Periplaneta americana . Journal of Insect Physiology23: 1407-1420 .
67.
Ritter, H., Martinez, T., and Schulten, K. 1992. Neural Computation and Self-Organizing Maps. An Introduction. Addison-Wesley, Reading, MA .
68.
Schmitz, J., and Haβfeld, G. 1989. The treading-on-tarsus reflex in stick insects: phase-dependence and modifications of the motor output during walking . Journal of Experimental Biology143: 373-388 .
69.
Schmidt, J., Fischer, H., and Büschges, A. 2001. Pattern generation for walking and searching movements of a stick insect leg. II. Control of motoneuronal activity . Journal of Neurophysiology85: 354-361 .
70.
Steinkühler, U., and Cruse, H. 1998. A holistic model for an internal representation to control the movement of a manipulator with redundant degrees of freedom . Biological Cybernetics79: 457-466 .
71.
Sutton, R., and Barto, A. G. 1999. Reinforcement Learning. An Introduction. MIT Press, Cambridge, MA .
72.
Tryba, A. K., and Ritzmann, R. E. 2000a. Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms . Journal of Neurophysiology83: 3323-3336 .
73.
Tryba, A. K., and Ritzmann, R. E. 2000b. Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern . Journal of Neurophysiology83: 3337-3350 .
74.
Ueno, N., and Kaneko, M. 1995. On a new contact sensing strategy for dynamic active antenna. In Proc. IEEE Int. Conf. on Robotics and Automation, 1120-1125.
75.
Ueno, N., Kaneko, M., and Svinin, M. 1996. Theoretical and experimental investigation on dynamic active antenna. In Proc. IEEE Int. Conf. on Robotics and Automation, 3557-3563.
76.
von Holst, E. 1943. Über relative Koordination bei Arthropoden . Pflügers Arch. 246: 847-865 .
77.
Watson, J. T., Ritzmann, R. E., Zill, S. N., and Pollack, A. J. 2002. Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics . Journal of Comparative Physiology A39-53 .
78.
Wilson, D.M. 1961. The central nervous control of locust flight . Journal of Experimental Biology38: 471-490 .
79.
Wolf, H., and 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 . Journal of Neurophysiology73: 1861-1875 .
80.
Wolf, H., and Pearson, K. G. 1987. Comparison of motor patterns in the intact and deafferented flight system of the locust. II. Intracellular recordings from flight motoneurons . Journal of Comparative Physiology A160: 269-279 .
81.
Wolf, H., and Pearson, K. G. 1988. Proprioceptive input patterns elevator activity in the locust flight system . Journal of Neurophysiology59: 1831-1853 .
82.
Wolpert, D. M., and Ghahramani, Z. 2000. Computational principles of movement neuroscience . Nature Neuroscience Supplement3: 1212-1217 .
83.
Zeil, J., Sandeman, R., and Sandeman, D. C. 1985. Tactile localisation: the function of active antennal movements in the crayfish Cherax destructor . Journal of Comparative Physiology A157: 607-617 .
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
