We report here an experimental-theoretical study of the features of the EMG activity of the iliopsoas (IP), tibialis anterior (TA), and gastrocnemius medialis (GM) muscles of the hindlimbs of decerebrate cats during walking induced by epidural spinal cord stimulation in various locomotor modes determined by the direction of movement of the treadmill belts: unidirectional walking in the forward (FW) and backward (BW) directions and bidirectional walking (BDW); an attempt was made to explain the data obtained in these experiments from the point of view of various central pattern generator (CPG) models. While maintaining the reciprocity of the operation of antagonist muscles during BDW, the activity of the TA and GM in BDW in oppositely directed limbs differed from each other: the activity of the TA and GM for the limb going backwards in BDW was similar to the activity of these muscles in unidirectional BW, and the activity of the TA and GM for limb moving forward during BDW was similar to the activity of these muscles during unidirectional FW. The patterns of IP activity of both limbs in BDW were similar, but IP activity was lower than for unidirectional FW and higher than for unidirectional BW. The stability of IP muscle activity was more variable than that of TA and GM. These data can be explained from the point of view of the operation of two-level CPG models, as well as a scheme for coordinating the CPG of different limbs, including reciprocal relationships between flexion half-centers and the influences of excitatory and inhibitory afferent signals on each component in the system in different phases of the locomotor cycle.
Similar content being viewed by others
References
Brown, T. G., “On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system,” J. Physiol., 48, No. 1, 18–46 (1914).
Brown, T. G., “The intrinsic factors in the act of progression in the mammal,” Proc. R. Soc. London B, 84, No. 572, 308–319 (1911).
Brown, T. G., “The phenomenon of ‘narcosis progression’ in mammals,” Proc. R. Soc. London B, 86, No. 586, 140–164 (1913).
Brownstone, R. M. and Wilson, J. M., “Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis,” Brain Res. Rev., 57, No. 1, 64–76 (2008).
Buford, J. A., Zernicke, R. F., and Smith, J. L., “Adaptive control for backward quadrupedal walking. I. Posture and hindlimb kinematics,” J. Neurophysiol., 64, No. 3, 745–755 (1990).
Burke, R. E., Degtyarenko, A. M., and Simon, E. S., “Patterns of locomotor drive to motoneurons and last-order interneurons: Clues to the structure of the CPG,” J. Neurophysiol., 86, No. 1, 447–462 (2001).
Choi, J. T. and Bastian, A. J., “Adaptation reveals independent control networks for human walking,” Nat. Neurosci., 10, No. 8, 1055–1062 (2007).
Collins, J. J. and Stewart, I. N., “Symmetry-breaking bifurcation: a possible mechanism for 2:1 frequency-locking in animal locomotion,” J. Math. Biol., 30, No. 8, 827–838 (1992).
Forssberg, H., Grillner, S., Halbertsma, J., and Rossignol, S., “The locomotion of the low spinal cat. II. Interlimb coordination,” Acta Physiol. Scand., 108, No. 3, 283–295 (1980).
Frigon, A., “The neural control of interlimb coordination during mammalian locomotion,” J. Neurophysiol., 117, No. 6, 2224–2241 (2017).
Frigon, A., Desrochers, É., Thibaudier, Y., et al., “Left–right coordination from simple to extreme conditions during split-belt locomotion in the chronic spinal adult cat,” J. Physiol., 595, No. 1, 341–361 (2017).
Gerasimenko, Y., Musienko, P., Bogacheva, I., et al., “Propriospinal bypass of the serotonergic system that can facilitate stepping,” J. Neurosci., 29, No. 17, 5681–5 (2009).
Grillner, S., “Biological pattern generation: The cellular and computational logic of networks in motion,” Neuron, 52, No. 5, 751–766 (2006).
Grillner, S., “Control of locomotion in bipeds, tetrapods, and fish,” in: Handbook of Physiology. The Nervous System II, Brookhart, M. (ed.), American Physiology Society, Bethesda, Rockville, MD, USA (1981), pp. 1179–1236.
Gurfinkel, V. S. and Shik, M. L., “The control of posture and locomotion,” in: Motor Control, Gydikov, A. et al. (eds.), Springer US (1974), pp. 217–234.
Halbertsma, J., “The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings,” Acta Physiol. Scand., Supplement, 521, 1–76 (1983).
Harnie, J., Audet, J., Klishko, A. N., et al., “The spinal control of backward locomotion,” J. Neurosci., 41, No. 4, 630–647 (2021).
Kato, M., “Chronically isolated lumbar half spinal cord, produced by hemisection and longitudinal myelotomy, generates locomotor activities of the ipsilateral hindlimb of the cat,” Neurosci. Lett., 98, 149–153 (1989).
Kato, M., “Longitudinal myelotomy of lumbar spinal cord has little effect on coordinated locomotor activities of bilateral hindlimbs of the chronic cats,” Neurosci. Lett., 93, 259–263 (1988).
Kim, S. A., Heinze, K. G., and Schwille, P., “Fluorescence correlation spectroscopy in living cells,” Nat. Methods, 4, No. 11, 963–973 (2007).
Kling, U. and Székely, G., “Simulation of rhythmic nervous activities,” Kybernetik, 5, No. 3, 89–103 (1968).
Kriellaars, D. J., Brownstone, R. M., Noga, B. R., and Jordan, L. M., “Mechanical entrainment of fictive locomotion in the decerebrate cat,” J. Neurophysiol., 71, No. 6, 2074–2086 (1994).
Kulagin, L. S. and Shik, M. L., “Interaction of symmetrical limbs in controlled locomotion,” Biofizika, 15, No. 1, 164–170 (1970).
Lafreniere-Roula, M. and McCrea, D. A., “Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provide clues to the organization of the mammalian central pattern generator,” J. Neurophysiol., 94, No. 2, 1120–1132 (2005).
Lam, T. and Pearson, K. G., “Proprioceptive modulation of hip flexor activity during the swing phase of locomotion in decerebrate cats,” J. Neurophysiol., 86, No. 3, 1321–1332 (2001).
Lundberg, A., “Half-centres revisited,” in: Regulatory Functions of the CNS. Principles of Motion and Organization: Proc. 28th Int. Congr. of Physiological Sciences, Budapest, Szentagothai, J. et al. (eds.), Pergamon, Budapest (1981), pp. 155–167.
Lyakhovetskii, V., Merkulyeva, N., Gorskii, O., and Musienko, P., “Simultaneous bidirectional hindlimb locomotion in decerebrate cats,” Sci. Rep., 11, No. 1, 3252 (2021).
McCrea, D. A. and Rybak, I. A., “Organization of mammalian locomotor rhythm and pattern generation,” Brain Res. Rev., 57, No. 1, 134–146 (2008).
Merkulyeva, N., Lyakhovetskii, V., Veshchitskii, A., et al., “Rostrocaudal distribution of the C-Fos-immunopositive spinal network defined by muscle activity during locomotion,” Brain Sci., 11, No. 1, 69 (2021).
Merkulyeva, N., Veshchitskii, A., Gorsky, O., et al., “Distribution of spinal neuronal networks controlling forward and backward locomotion,” J. Neurosci., 38, No. 20, 4695–4707 (2018).
Molkov, Y. I., Bacak, B. J., Talpalar, A. E., and Rybak, I. A., “Mechanisms of left-right coordination in mammalian locomotor pattern generation circuits: A mathematical modeling view,” PLoS Comput. Biol., 11, No. 5, e1004270 (2015).
Musienko, P., Brand, R. V. D., Märzendorfer, O., et al., “Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries,” J. Neurosci., 31, No. 25, 9264–9278 (2011).
Musienko, P., Courtine, G., Tibbs, J. E., et al., “Somatosensory control of balance during locomotion in decerebrated cat,” J. Neurophysiol., 107, No. 8, 2072–2082 (2012).
Pearson, K. G. and Duysens, J., “Function of segmental reflexes in the control of stepping in cockroaches and cats,” in: Neural Control of Locomotion. Advances in Behavioral Biology, Herman, R. M. et al. (eds.), Springer US (1976), pp. 519–537.
Pearson, K. G., “Proprioceptive regulation of locomotion,” Curr. Opin. Neurobiol., 5, No. 6, 786–791 (1995).
Pearson, K. G., “Role of sensory feedback in the control of stance duration in walking cats,” Brain Res. Rev., 57, No. 1, 222–227 (2008).
Pearson, K. G., Fourtner, C. R., and Wong, R. K., “Nervous control of walking in the cockroach,” in: Control of Posture and Locomotion, Advances in Behavioral Biology, Stein, R. B. et al. (eds.), Springer US (1973), pp. 495–514.
Pratt, C. A., Buford, J. A., and Smith, J. L., “Adaptive control for backward quadrupedal walking V. Mutable activation of bifunctional thigh muscles,” J. Neurophysiol., 75, No. 2, 832–842 (1996).
Press, W. H., Teukolsky, S. A., Vetterling, W. T., and Flannery, B. P., “Statistical Description of Data,” in: Numerical recipes in C++. The Art of Scientific Computing, Press, W. H. et al. (eds.), Cambridge University Press (2007).
Rossignol, S., Dubuc, R., and Gossard, J.-P., “Dynamic sensorimotor interactions in locomotion,” Physiol. Rev., 86, No. 1, 89–154 (2006).
Rybak, I. A., Dougherty, K. J., and Shevtsova, N. A., “Organization of the mammalian locomotor CPG: Review of computational model and circuit architectures based on genetically identified spinal interneurons,” eNeuro, 2, No. 5, 1–20 (2015).
Sherrington, C. S., “Flexion-refl ex of the limb, crossed extension-reflex, and reflex stepping and standing,” J. Physiol., 40, No. 1–2, 28–121 (1910).
Shik, M. L. and Orlovsky, G. N., “Neurophysiology of locomotor automatism,” Physiol. Rev., 56, No. 3, 465–501 (1976).
Shik, M. L., Movement Physiology, Nauka, Leningrad (1976).
Shkorbatova, P. Y., Lyakhovetskii, V. A., Merkulyeva, N. S., et al., “Prediction algorithm of the cat spinal segments lengths and positions in relation to the vertebrae,” Anat. Rec., 302, No. 9, 1628–1637 (2019).
Smith, J. L. and Carlson-Kuhta, P., “Unexpected motor patterns for hindlimb muscles during slope walking in the cat,” J. Neurophysiol., 74, No. 5, 2211–2215 (1995).
Stafford, F. S. and Barnwell, G. M., “Mathematical models of central pattern generators in locomotion,” J. Mot. Behav., 17, No. 1, 3–26 (1985).
Yang, Y.-R., Yen J.-G., Wang, R.-Y., et al., “Gait outcomes after additional backward walking training in patients with stroke: a randomized controlled trial,” Clin. Rehabil., 19, No. 3, 264–273 (2005).
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 72, No. 2, pp. 259–273, March–April, 2022.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Veshchitskii, A.A., Lyakhovetskii, V.A., Gorskii, O.V. et al. What Can Bidirectional Walking Tell Us about Central Pattern Generators?. Neurosci Behav Physi 52, 1277–1286 (2022). https://doi.org/10.1007/s11055-023-01357-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-023-01357-0