Skip to main content
Log in

Sensorimotor Interactions During Locomotion: Principles Derived from Biological Systems

  • Published:
Autonomous Robots Aims and scope Submit manuscript

Abstract

Rhythmic movements in biological systems are produced in part by central circuits called central pattern generators (CPGs). For example, locomotion in vertebrates derives from the spinal CPG with activity initiated by the brain and controlled by sensory feedback. Sensory feedback is traditionally viewed as controlling CPGs cycle by cycle, with the brain commanding movements on a top down basis. We present an alternative view which in sensory feedback alters the properties of the CPG on a fast as well as a slow time scale. The CPG, in turn, provides feedforward filtering of the sensory feedback. This bidirectional interaction is widespread across animals, suggesting it is a common feature of motor systems, and, therefore, might offer a new way to view sensorimotor interactions in all systems including robotic systems. Bidirectional interactions are also apparent between the cerebral cortex and the CPG. The motor cortex doesn't simply command muscle contractions, but rather operates with the CPG to produce adaptively structured movements. To facilitate these adaptive interactions, the motor cortex receives feedback from the CPG that creates a temporal activity pattern mirroring the spinal motor output during locomotion. Thus, the activity of the motor cortical cells is shaped by the spinal pattern generator as they drive motor commands. These common features of CPG structure and function are suggested as offering a new perspective for building robotic systems. CPGs offer a potential for adaptive control, especially when combined with the principles of sensorimotor integration described here.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Andersson, O. and Grillner, S. 1983. Peripheral control of the cat's step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during “fictive locomotion”. Acta Physiol. Scand., 118:229-239.

    Google Scholar 

  • Armstrong, D.M. and Drew, T. 1985. Forelimb electromyographic responses to motor cortex stimulation during locomotion in the cat. J. Physiol. (Lond), 367:327-351.

    Google Scholar 

  • Beloozerova, I.N. and Sirota, M.G. 1998. Cortically controlled gait adjustments in the cat. Ann. N Y Acad. Sci., 860:550-553.

    Google Scholar 

  • Beloozerova, I.N. and Sirota, M.G. 1993. The role of the motor cortex in the control of vigour of locomotor movements in the cat. J. Physiol. (Lond), 461:27-46.

    Google Scholar 

  • Buschges, A., Ramirez, J.-M., and Pearson, K. 1991. Reorganization of sensory regulation of locust flight after partial deafferentation. J. Neurobiol., 23:31-43.

    Google Scholar 

  • Cohen, A.H., Ermentrout, G.B., Kiemel, T., Kopell, N., Sigvardt, K., and Williams, T. 1992. Modelling of intersegmental coordination in the lamprey central pattern or for locomotion. TINS, 15:434-438.

    Google Scholar 

  • Dubuc, R., Cabelguen, J.-M., and Rossignol, S. 1988. Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. J. Neurophysiol., 60:2014-2037.

    Google Scholar 

  • Dykstra, S., Kiemel, T., and Cohen, A.H. 1995. Analysis of transient behaviors in the lamprey locomotor central pattern generator during initiation and termination of mechanical entrainment. Soc. Neurosci. Abst., 21.

  • Forssberg, H. 1979. On integrative motor functions in the cat's spinal cord. Acta Physiol. Scand., 474:3-43.

    Google Scholar 

  • Forssberg, H., Grillner, S., and Rossignol, S. 1977. Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Res., 132:121-139.

    Google Scholar 

  • Gossard, J., Cabelguen, J., and Rossignol, S. 1991. An intracellular study of muscle primary afferents during fictive locomotion in the cat. J. Neurophysiol., 65:914-926.

    Google Scholar 

  • Grillner, S., Wallén, P., and Brodin, L. 1991. Neuronal network generating locomotor behavior in lamprey: Circuitry, transmitters, membrane properties and simulation. Ann. Rev. Neurosci., 14:169-199.

    Google Scholar 

  • Grillner, S. and Wallén, P. 1982. On peripheral control mechanisms acting on the central pattern generators for swimming in the dogfish. Exp. Biol., 98:1-22.

    Google Scholar 

  • Grillner, S. and Zangger, P. 1979. On the central generation of locomotion in the low spinal cat. Exp. Brain. Res., 34(2):241-261.

    Google Scholar 

  • Hiebert, G., Gorassini, M., Jiang, W., Prochazka, A., and Pearson, K. 1994. Corrective responses to loss of ground support during walking II, comparison of intact and chronic spinal cats. J. Neurophys. 71:611-622.

    Google Scholar 

  • Hiebert, G., Whelan, P., Prochazka, A., and Pearson, K. 1996. Contribution of hind limb flexor muscle afferents to the timing of phase transitions in the cat step cycle. J. Neurophysiol., 75:1126-1137.

    Google Scholar 

  • Jankowska, E. and Lundberg, A. 1981. Interneurones in the spinal cord. TINS, 4:230-233.

    Google Scholar 

  • Kiemel, T. and Cohen, A. 1998. Estimation of coupling strength in regenerated lamprey spinal cords based on a stochastic phase model. J. Computat. Neurosci., 5:267-284.

    Google Scholar 

  • Lewis, M.A. 1999. Sensory and visually mediated gait adaptation in a quadruped robot. Autonomous Robots, Accepted.

  • Libersat, F., Levy, A., and Camhi, J. 1989. Multiple feedback loops in the flying cockroach: excitation of dorsal and inhibitionof the ventral giant interneurons. J. Comp. Physiol., A 165:651-688.

    Google Scholar 

  • McCrea, D. 1996. Supraspinal and segmental interactions. Can. J. of Phys. and Pharmacol., 74:513-517.

    Google Scholar 

  • McNaughton, B., Mizumori, C., Barnes, C., Leonard, B., Marquis, M., and Green, E. 1994. Cortical representation of motion during unrestrained spatial navigation in the rat. Cerebral Cortex, 4:27-39.

    Google Scholar 

  • Mellen, N., Kiemel, T., and Cohen, A.H. 1995. Correlational analysis of fictive swimming in the lamprey reveals strong functional intersegmental coupling. J. Neurophysiol., 73:1020-1030.

    Google Scholar 

  • Nussbaum, M., El Manira, A., Gossard, J.-P., and Rossignol, S. 1996. Presynaptic mechanisms during rhythmic activity in vertebrates and invertebrates. In Neurons; Networks; and Motor Behavior, P.S.G. Stein, S. Grillner, A.I. Selverston, and D.G. Stuart (Eds.), Cambridge: MIT Press.

    Google Scholar 

  • Ramirez, J. and Pearson, K. 1995. Alteration of bursting properties in interneurons during locust flight. J. Neurophysiol., 70:2148-2160.

    Google Scholar 

  • Rossignol, S., Beloozerova, I, Gossard, J.-P., and Dubuc, R. 1998. Presynaptic mechanisms during locomotion. In Presynaptic Inhibition and Neural Control, P. Rudomin, R. Romo, L. Mendell (Eds.), Oxford Univ. Press, pp. 385-397.

  • Rossignol, S., Lund, J.P., and Drew, T. 1988. The role of sensory inputs in reguating patterns of rhythmical movements in higher vertebrates: A comparison between locomotion, respiration and mastication. In Neural Control of Rhythmic Movement in Vertebrates, A.H. Cohen, S. Rossignol, and S. Grillner (Eds.), John Wiley and Sons, Inc.: New York, pp. 201-284.

    Google Scholar 

  • Sillar, K. 1991. Spinal pattern generation and sensory gating mechanisms. Curr. Opin. Neurobiol., 1:583-589.

    Google Scholar 

  • Sharp, A., Skinner, F., and Marder, E., Mechanisms of oscillation in dynamic clamp constructed two-cell half-center circuits. J. Neurophysiol., 76:867-883.

  • Vinay, L., Barthe, J., and Grillner, S. 1996. Central modulation of stretch receptor neurons during fictive locomotion in lamprey. J. Neurophysiol., 76:1224-1235.

    Google Scholar 

  • Weimann, J., Meyrand, P., and Marder, E. 1991, Neurons that form multiple pattern generators: Identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J. of Neuroanatomy, 65:111-122.

    Google Scholar 

  • Wolf, H. and Burrows, M. 1995. Proprioceptive sensory neurons of a locust leg receive rhythmic presynpatic inhibition during walking. J. Neurosci., 15:5623-5636.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cohen, A.H., Boothe, D.L. Sensorimotor Interactions During Locomotion: Principles Derived from Biological Systems. Autonomous Robots 7, 239–245 (1999). https://doi.org/10.1023/A:1008920420634

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1008920420634

Navigation