Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics

Bicanski A, Ryczko D, Knuesel J, Harischandra N, Charrier V, Ekeberg Ö, Cabelguen J-M, Ijspeert AJ (2013)
Journal of Biological Cybernetics 107(5): 545-564.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ; ; ;
Abstract / Bemerkung
Vertebrate animals exhibit impressive locomotor skills. These locomotor skills are due to the complex interactions between the environment, the musculo-skeletal system and the central nervous system, in particular the spinal locomotor circuits. We are interested in decoding these interactions in the salamander, a key animal from an evolutionary point of view. It exhibits both swimming and stepping gaits and is faced with the problem of producing efficient propulsive forces using the same musculo-skeletal system in two environments with significant physical differences in density, viscosity and gravitational load. Yet its nervous system remains comparatively simple. Our approach is based on a combination of neurophysiological experiments, numerical modeling at different levels of abstraction, and robotic validation using an amphibious salamander-like robot. This article reviews the current state of our knowledge on salamander locomotion control, and presents how our approach has allowed us to obtain a first conceptual model of the salamander spinal locomotor networks. The model suggests that the salamander locomotor circuit can be seen as a lamprey-like circuit controlling axial movements of the trunk and tail, extended by specialized oscillatory centers controlling limb movements. The interplay between the two types of circuits determines the mode of locomotion under the influence of sensory feedback and descending drive, with stepping gaits at low drive, and swimming at high drive.
Erscheinungsjahr
Zeitschriftentitel
Journal of Biological Cybernetics
Band
107
Zeitschriftennummer
5
Seite
545-564
ISSN
eISSN
PUB-ID

Zitieren

Bicanski A, Ryczko D, Knuesel J, et al. Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Journal of Biological Cybernetics. 2013;107(5):545-564.
Bicanski, A., Ryczko, D., Knuesel, J., Harischandra, N., Charrier, V., Ekeberg, Ö., Cabelguen, J. - M., et al. (2013). Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Journal of Biological Cybernetics, 107(5), 545-564. doi:10.1007/s00422-012-0543-1
Bicanski, A., Ryczko, D., Knuesel, J., Harischandra, N., Charrier, V., Ekeberg, Ö., Cabelguen, J. - M., and Ijspeert, A. J. (2013). Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Journal of Biological Cybernetics 107, 545-564.
Bicanski, A., et al., 2013. Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Journal of Biological Cybernetics, 107(5), p 545-564.
A. Bicanski, et al., “Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics”, Journal of Biological Cybernetics, vol. 107, 2013, pp. 545-564.
Bicanski, A., Ryczko, D., Knuesel, J., Harischandra, N., Charrier, V., Ekeberg, Ö., Cabelguen, J.-M., Ijspeert, A.J.: Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Journal of Biological Cybernetics. 107, 545-564 (2013).
Bicanski, A., Ryczko, D., Knuesel, J., Harischandra, Nalin, Charrier, V., Ekeberg, Ö., Cabelguen, J.-M., and Ijspeert, A.J. “Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics”. Journal of Biological Cybernetics 107.5 (2013): 545-564.

7 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

A new model of the spinal locomotor networks of a salamander and its properties.
Liu Q, Yang H, Zhang J, Wang J., Biol Cybern 112(4), 2018
PMID: 29790009
Development and Training of a Neural Controller for Hind Leg Walking in a Dog Robot.
Hunt A, Szczecinski N, Quinn R., Front Neurorobot 11(), 2017
PMID: 28420977
Flexibility of the axial central pattern generator network for locomotion in the salamander.
Ryczko D, Knüsel J, Crespi A, Lamarque S, Mathou A, Ijspeert AJ, Cabelguen JM., J Neurophysiol 113(6), 2015
PMID: 25540227
Modular functional organisation of the axial locomotor system in salamanders.
Cabelguen JM, Charrier V, Mathou A., Zoology (Jena) 117(1), 2014
PMID: 24290785
Fictive rhythmic motor patterns produced by the tail spinal cord in salamanders.
Charrier V, Cabelguen JM., Neuroscience 255(), 2013
PMID: 24161283

121 References

Daten bereitgestellt von Europe PubMed Central.


AUTHOR UNKNOWN, 0

MA, J Comp Physiol [A] 177(), 1995
Kinematics of level terrestrial and underwater walking in the California newt, Taricha torosa.
Ashley-Ross MA, Lundin R, Johnson KL., J Exp Zool A Ecol Genet Physiol 311(4), 2009
PMID: 19266497
Behavior of hindbrain neurons during the transition from rest to evoked locomotion in a newt.
Bar-Gad I, Kagan I, Shik ML., Prog. Brain Res. 123(), 1999
PMID: 10635724
From swimming to walking: a single basic network for two different behaviors.
Bem T, Cabelguen JM, Ekeberg O, Grillner S., Biol Cybern 88(2), 2003
PMID: 12567223
Twisting and bending: the functional role of salamander lateral hypaxial musculature during locomotion.
Bennett WO, Simons RS, Brainerd EL., J. Exp. Biol. 204(Pt 11), 2001
PMID: 11441039
Modeling axial spinal segments of the salamander central pattern generator for locomotion.
Bicanski A, Ryczko D, Cabelguen J, Ijspeert AJ., BMC Neurosci 12(Suppl 1), 2011
PMID: PMC3240253
New perspectives on spinal motor systems.
Bizzi E, Tresch MC, Saltiel P, d'Avella A., Nat. Rev. Neurosci. 1(2), 2000
PMID: 11252772
Combining modules for movement.
Bizzi E, Cheung VC, d'Avella A, Saltiel P, Tresch M., Brain Res Rev 57(1), 2007
PMID: 18029291

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
Axial dynamics during locomotion in vertebrates lesson from the salamander.
Cabelguen JM, Ijspeert A, Lamarque S, Ryczko D., Prog. Brain Res. 187(), 2010
PMID: 21111206
Fast and slow locomotor burst generation in the hemispinal cord of the lamprey.
Cangiano L, Grillner S., J. Neurophysiol. 89(6), 2003
PMID: 12611971

DR, J Exp Biol 180(), 1993

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling.
Chevallier S, Jan Ijspeert A, Ryczko D, Nagy F, Cabelguen JM., Brain Res Rev 57(1), 2007
PMID: 17920689
Recovery of bimodal locomotion in the spinal-transected salamander, Pleurodeles waltlii.
Chevallier S, Landry M, Nagy F, Cabelguen JM., Eur. J. Neurosci. 20(8), 2004
PMID: 15450078
Identification, localization, and modulation of neural networks for walking in the mudpuppy (Necturus maculatus) spinal cord.
Cheng J, Stein RB, Jovanovic K, Yoshida K, Bennett DJ, Han Y., J. Neurosci. 18(11), 1998
PMID: 9592106
Differential distribution of interneurons in the neural networks that control walking in the mudpuppy (Necturus maculatus) spinal cord.
Cheng J, Jovanovic K, Aoyagi Y, Bennett DJ, Han Y, Stein RB., Exp Brain Res 145(2), 2002
PMID: 12110959

AUTHOR UNKNOWN, 0
Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion.
Cohen AH, Ermentrout GB, Kiemel T, Kopell N, Sigvardt KA, Williams TL., Trends Neurosci. 15(11), 1992
PMID: 1281350

AUTHOR UNKNOWN, 0

S, Proc Ned Akad Wetten C 71(), 1968

K, Neth J Zool 46(), 1996
Low dimensionality of supraspinally induced force fields.
d'Avella A, Bizzi E., Proc. Natl. Acad. Sci. U.S.A. 95(13), 1998
PMID: 9636215
Activity of reticulospinal neurons during locomotion in the freely behaving lamprey.
Deliagina TG, Zelenin PV, Fagerstedt P, Grillner S, Orlovsky GN., J. Neurophysiol. 83(2), 2000
PMID: 10669499

AUTHOR UNKNOWN, 0
Fictive rhythmic motor patterns induced by NMDA in an in vitro brain stem-spinal cord preparation from an adult urodele.
Delvolve I, Branchereau P, Dubuc R, Cabelguen JM., J. Neurophysiol. 82(2), 1999
PMID: 10444700
Locomotor primitives in newborn babies and their development.
Dominici N, Ivanenko YP, Cappellini G, d'Avella A, Mondi V, Cicchese M, Fabiano A, Silei T, Di Paolo A, Giannini C, Poppele RE, Lacquaniti F., Science 334(6058), 2011
PMID: 22096202

R, 2009
Initiation of locomotion in lampreys.
Dubuc R, Brocard F, Antri M, Fenelon K, Gariepy JF, Smetana R, Menard A, Le Ray D, Viana Di Prisco G, Pearlstein E, Sirota MG, Derjean D, St-Pierre M, Zielinski B, Auclair F, Veilleux D., Brain Res Rev 57(1), 2007
PMID: 17916380

JL, 1977
Locomotor control in macaque monkeys.
Eidelberg E, Walden JG, Nguyen LH., Brain 104(Pt 4), 1981
PMID: 7326562

Ö, Biol Cybern 69(), 1993
Lateral turns in the Lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns.
Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, Ullen F., J. Neurophysiol. 86(5), 2001
PMID: 11698516

L, J Exp Biol 162(), 1992
Convergent force fields organized in the frog's spinal cord.
Giszter SF, Mussa-Ivaldi FA, Bizzi E., J. Neurosci. 13(2), 1993
PMID: 8426224

AUTHOR UNKNOWN, 0
Mechanosensitive neurons in the spinal cord of the lamprey.
Grillner S, McClellan A, Sigvardt K., Brain Res. 235(1), 1982
PMID: 7188321
The edge cell, a possible intraspinal mechanoreceptor.
Grillner S, Williams T, Lagerback PA., Science 223(4635), 1984
PMID: 6691161

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
Neuroscience. Human locomotor circuits conform.
Grillner S., Science 334(6058), 2011
PMID: 22096178

L, J Experim Biol 204(), 2001
Spinal cord neuron classes in embryos of the smooth newt Triturus vulgaris: a horseradish peroxidase and immunocytochemical study.
Harper CE, Roberts A., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 340(1291), 1993
PMID: 8099742

AUTHOR UNKNOWN, 0
Sensory feedback plays a significant role in generating walking gait and in gait transition in salamanders: a simulation study.
Harischandra N, Knuesel J, Kozlov A, Bicanski A, Cabelguen JM, Ijspeert A, Ekeberg O., Front Neurorobot 5(), 2011
PMID: 22069388
Intersegmental coordination of rhythmic motor patterns.
Hill AA, Masino MA, Calabrese RL., J. Neurophysiol. 90(2), 2003
PMID: 12904484
From swimming to walking with a salamander robot driven by a spinal cord model.
Ijspeert AJ, Crespi A, Ryczko D, Cabelguen JM., Science 315(5817), 2007
PMID: 17347441
Electrically evoked walking and fictive locomotion in the chick.
Jacobson RD, Hollyday M., J. Neurophysiol. 48(1), 1982
PMID: 7119848

AUTHOR UNKNOWN, 0

J, BMC Neurosci 12(Suppl. 1), 2011

N, SIAM J Appl Math 51(), 1991
Simple cellular and network control principles govern complex patterns of motor behavior.
Kozlov A, Huss M, Lansner A, Kotaleski JH, Grillner S., Proc. Natl. Acad. Sci. U.S.A. 106(47), 2009
PMID: 19901329
A hemicord locomotor network of excitatory interneurons: a simulation study.
Kozlov AK, Lansner A, Grillner S, Kotaleski JH., Biol Cybern 96(2), 2006
PMID: 17180687

AUTHOR UNKNOWN, 0
Chapter 4--supraspinal control of locomotion: the mesencephalic locomotor region.
Le Ray D, Juvin L, Ryczko D, Dubuc R., Prog. Brain Res. 188(), 2011
PMID: 21333802
Descending pathways in motor control.
Lemon RN., Annu. Rev. Neurosci. 31(), 2008
PMID: 18558853
Learning from the spinal cord.
Loeb GE., J. Physiol. (Lond.) 533(Pt 1), 2001
PMID: 11351019

AUTHOR UNKNOWN, 0
Organization of mammalian locomotor rhythm and pattern generation.
McCrea DA, Rybak IA., Brain Res Rev 57(1), 2007
PMID: 17936363
Spike-frequency adapting neural ensembles: beyond mean adaptation and renewal theories.
Muller E, Buesing L, Schemmel J, Meier K., Neural Comput 19(11), 2007
PMID: 17883347
Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems.
Mullins OJ, Hackett JT, Buchanan JT, Friesen WO., Prog. Neurobiol. 93(2), 2010
PMID: 21093529
Linear combinations of primitives in vertebrate motor control.
Mussa-Ivaldi FA, Giszter SF, Bizzi E., Proc. Natl. Acad. Sci. U.S.A. 91(16), 1994
PMID: 8052615
Common principles of motor control in vertebrates and invertebrates.
Pearson KG., Annu. Rev. Neurosci. 16(), 1993
PMID: 8460894
Assessing sensory function in locomotor systems using neuro-mechanical simulations.
Pearson K, Ekeberg O, Buschges A., Trends Neurosci. 29(11), 2006
PMID: 16956675
From salamanders to mammals: continuity in musculoskeletal function during locomotion.
Peters SE, Goslow GE Jr., Brain Behav. Evol. 22(4), 1983
PMID: 6616172

AUTHOR UNKNOWN, 0

P, Proc Ned Akad Wetten C 67(), 1964
Pharmacological activation and modulation of the central pattern generator for locomotion in the cat.
Rossignol S, Chau C, Brustein E, Giroux N, Bouyer L, Barbeau H, Reader TA., Ann. N. Y. Acad. Sci. 860(), 1998
PMID: 9928324
Dynamic sensorimotor interactions in locomotion.
Rossignol S, Dubuc R, Gossard JP., Physiol. Rev. 86(1), 2006
PMID: 16371596

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0
Segmental oscillators in axial motor circuits of the salamander: distribution and bursting mechanisms.
Ryczko D, Charrier V, Ijspeert A, Cabelguen JM., J. Neurophysiol. 104(5), 2010
PMID: 20810687
Rhythmogenesis in axial locomotor networks: an interspecies comparison.
Ryczko D, Dubuc R, Cabelguen JM., Prog. Brain Res. 187(), 2010
PMID: 21111209
Spinal cord modular organization and rhythm generation: an NMDA iontophoretic study in the frog.
Saltiel P, Tresch MC, Bizzi E., J. Neurophysiol. 80(5), 1998
PMID: 9819246
Marginal neurons in the urodele spinal cord and the associated denticulate ligaments.
Schroeder DM, Egar MW., J. Comp. Neurol. 301(1), 1990
PMID: 1706360
[Control of walking and running by means of electric stimulation of the midbrain]
Shik ML, Severin FV, Orlovskii GN., Biofizika 11(4), 1966
PMID: 6000625
The mesencephalic locomotor region (MLR) in the rat.
Skinner RD, Garcia-Rill E., Brain Res. 323(2), 1984
PMID: 6525525
Stimulation of the pontomedullary reticular formation initiates locomotion in decerebrate birds.
Steeves JD, Sholomenko GN, Webster DM., Brain Res. 401(2), 1987
PMID: 3815097

AUTHOR UNKNOWN, 0
The activity pattern of limb muscles in freely moving normal and deafferented newts.
Szekely G, Czeh G, Voros G., Exp Brain Res 9(1), 1969
PMID: 5808480
Interactions between internal forces, body stiffness, and fluid environment in a neuromechanical model of lamprey swimming.
Tytell ED, Hsu CY, Williams TL, Cohen AH, Fauci LJ., Proc. Natl. Acad. Sci. U.S.A. 107(46), 2010
PMID: 21037110

AUTHOR UNKNOWN, 0

P, Proc Am Control Conf 5(), 1997

AUTHOR UNKNOWN, 0
A comparison of intact and in-vitro locomotion in an adult amphibian.
Wheatley M, Edamura M, Stein RB., Exp Brain Res 88(3), 1992
PMID: 1587318

AUTHOR UNKNOWN, 0

AUTHOR UNKNOWN, 0

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 23430277
PubMed | Europe PMC

Suchen in

Google Scholar