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What Can Bidirectional Walking Tell Us about Central Pattern Generators?

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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.

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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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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).

    Article  Google Scholar 

  • Brown, T. G., “The phenomenon of ‘narcosis progression’ in mammals,” Proc. R. Soc. London B, 86, No. 586, 140–164 (1913).

    Article  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • Choi, J. T. and Bastian, A. J., “Adaptation reveals independent control networks for human walking,” Nat. Neurosci., 10, No. 8, 1055–1062 (2007).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • Frigon, A., “The neural control of interlimb coordination during mammalian locomotion,” J. Neurophysiol., 117, No. 6, 2224–2241 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grillner, S., “Biological pattern generation: The cellular and computational logic of networks in motion,” Neuron, 52, No. 5, 751–766 (2006).

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • Kim, S. A., Heinze, K. G., and Schwille, P., “Fluorescence correlation spectroscopy in living cells,” Nat. Methods, 4, No. 11, 963–973 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Kling, U. and Székely, G., “Simulation of rhythmic nervous activities,” Kybernetik, 5, No. 3, 89–103 (1968).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • Kulagin, L. S. and Shik, M. L., “Interaction of symmetrical limbs in controlled locomotion,” Biofizika, 15, No. 1, 164–170 (1970).

    CAS  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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).

    Article  PubMed  PubMed Central  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shik, M. L. and Orlovsky, G. N., “Neurophysiology of locomotor automatism,” Physiol. Rev., 56, No. 3, 465–501 (1976).

    Article  CAS  PubMed  Google Scholar 

  • Shik, M. L., Movement Physiology, Nauka, Leningrad (1976).

    Google Scholar 

  • 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).

    Article  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • Stafford, F. S. and Barnwell, G. M., “Mathematical models of central pattern generators in locomotion,” J. Mot. Behav., 17, No. 1, 3–26 (1985).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

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Correspondence to N. S. Merkulyeva.

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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 72, No. 2, pp. 259–273, March–April, 2022.

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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

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