[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Springer Nature Link
Log in

Evaluating functional roles of phase resetting in generation of adaptive human bipedal walking with a physiologically based model of the spinal pattern generator

  • Original Paper
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

The central pattern generators (CPGs) in the spinal cord strongly contribute to locomotor behavior. To achieve adaptive locomotion, locomotor rhythm generated by the CPGs is suggested to be functionally modulated by phase resetting based on sensory afferent or perturbations. Although phase resetting has been investigated during fictive locomotion in cats, its functional roles in actual locomotion have not been clarified. Recently, simulation studies have been conducted to examine the roles of phase resetting during human bipedal walking, assuming that locomotion is generated based on prescribed kinematics and feedback control. However, such kinematically based modeling cannot be used to fully elucidate the mechanisms of adaptation. In this article we proposed a more physiologically based mathematical model of the neural system for locomotion and investigated the functional roles of phase resetting. We constructed a locomotor CPG model based on a two-layered hierarchical network model of the rhythm generator (RG) and pattern formation (PF) networks. The RG model produces rhythm information using phase oscillators and regulates it by phase resetting based on foot-contact information. The PF model creates feedforward command signals based on rhythm information, which consists of the combination of five rectangular pulses based on previous analyses of muscle synergy. Simulation results showed that our model establishes adaptive walking against perturbing forces and variations in the environment, with phase resetting playing important roles in increasing the robustness of responses, suggesting that this mechanism of regulation may contribute to the generation of adaptive human bipedal locomotion.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aoi S, Ogihara N, Sugimoto Y, Tsuchiya K (2008) Simulating adaptive human bipedal locomotion based on phase resetting using foot-contact information. Adv Robot 22: 1697–1713

    Article  Google Scholar 

  • Burke RE, Degtyarenko AM, Simon ES (2001) Patterns of locomotor drive to motoneurons and last-order interneurons: Clues to the structure of the CPG. J Neurophysiol 86: 447–462

    CAS  PubMed  Google Scholar 

  • Conway BA, Hultborn H, Kiehn O (1987) Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res 68: 643–656

    Article  CAS  PubMed  Google Scholar 

  • Danna-dos-Santos A, Slomka K, Zatsiorsky VM, Latash ML (2007) Muscle modes and synergies during voluntary body sway. Exp Brain Res 179: 533–550

    Article  PubMed  Google Scholar 

  • d’Avella A, Bizzi E (2005) Shared and specific muscle synergies in natural motor behaviors. Proc Natl Acad Sci USA 102(8): 3076–3081

    Article  PubMed  Google Scholar 

  • d’Avella A, Saltiel P, Bizzi E (2003) Combinations of muscle synergies in the construction of a natural motor behavior. Nat Neurosci 6: 300–308

    Article  PubMed  Google Scholar 

  • Davy DT, Audu ML (1987) A dynamic optimization technique for predicting muscle forces in the swing phase of gait. J Biomech 20(2): 187–201

    Article  CAS  PubMed  Google Scholar 

  • Drew T, Kalaska J, Krouchev N (2008) Muscle synergies during locomotion in the cat: a model for motor cortex control. J Physiol 586(5): 1239–1245

    Article  CAS  PubMed  Google Scholar 

  • Duysens J (1977) Fluctuations in sensitivity to rhythm resetting effects during the cat’s step cycle. Brain Res 133(1): 190–195

    Article  CAS  PubMed  Google Scholar 

  • Duysens J, Pearson KG (1980) Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187: 321–332

    Article  CAS  PubMed  Google Scholar 

  • Ekeberg Ö, Pearson K (2005) Computer simulation of stepping in the hind legs of the cat: an examination of mechanisms regulating the stance-to-swing transition. J Neurophysiol 94: 4256–4268

    Article  PubMed  Google Scholar 

  • Frigon A, Rossignol S (2006) Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95: 607–627

    Article  PubMed  Google Scholar 

  • Fuglevand AJ, Winter DA (1993) Models of recruitment and rate coding organization in motor-unit pools. J Neurophysiol 70(6): 2470–2488

    CAS  PubMed  Google Scholar 

  • Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev 55(2): 247–304

    Article  CAS  PubMed  Google Scholar 

  • Grillner S, Rossignol S (1978) On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 146: 269–277

    Article  CAS  PubMed  Google Scholar 

  • Guertin PA (2009) The mammalian central pattern generator for locomotion. Brain Res Rev 62: 45–56

    Article  PubMed  Google Scholar 

  • Guertin P, Angel MJ, Perreault M-C, McCrea DA (1995) Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J Physiol 487(1): 197–209

    CAS  PubMed  Google Scholar 

  • Hiebert GW, Whelan PJ, Prochazka A, Pearson KG (1996) Contribution of hindlimb flexor muscle afferents to the timing of phase transitions in the cat step cycle. J Neurophysiol 75: 1126–1137

    CAS  PubMed  Google Scholar 

  • Hultborn H, Nielsen JB (2007) Spinal control of locomotion—from cat to man. Acta Physiol 189: 111–121

    Article  CAS  Google Scholar 

  • Inman VT (1953) The pattern of muscular activity in the lower extremity during walking (Technical Report Series II, No. 25), Prosthetic Devices Research Project, Institute of Engineering Research, University of California, Berkeley, CA

  • Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556: 267–282

    Article  CAS  PubMed  Google Scholar 

  • Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2005) Coordination of locomotion with voluntary movements in humans. J Neurosci 25(31): 7238–7253

    Article  CAS  PubMed  Google Scholar 

  • Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor control programs and walking. Neuroscientist 12(4): 339–348

    Article  PubMed  Google Scholar 

  • Ijspeert AJ (2001) A connectionist central pattern generator for the aquatic and terrestrial gaits of a simulated salamander. Biol Cybern 84: 331–348

    Article  CAS  PubMed  Google Scholar 

  • Jo S (2008) Hypothetical neural control of human bipedal walking with voluntary modulation. Med Biol Eng Comput 46: 179–193

    Article  PubMed  Google Scholar 

  • Jo S, Massaquoi SG (2007) A model of cerebrocerebello-spinomuscular interaction in the sagittal control of human walking. Biol Cybern 96: 279–307

    Article  PubMed  Google Scholar 

  • Lafreniere-Roula M, McCrea DA (2005) Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provideclues to the organization of the mammalian central pattern generator. J Neurophysiol 94: 1120–1132

    Article  PubMed  Google Scholar 

  • McCrea DA, Rybak IA (2008) Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57: 134–146

    Article  PubMed  Google Scholar 

  • Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR (2007) Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci 26: 275–295

    Article  CAS  PubMed  Google Scholar 

  • Nomura T, Kawa K, Suzuki Y, Nakanishi M, Yamasaki T (2009) Dynamic stability and phase resetting during biped gait. Chaos 19: 026103

    Article  PubMed  Google Scholar 

  • Ogihara N, Yamazaki N (2001) Generation of human bipedal locomotion by a bio-mimetic neuro-musculo-skeletal model. Biol Cybern 84: 1–11

    Article  CAS  PubMed  Google Scholar 

  • Orlovsky GN, Deliagina T, Grillner S (1999) Neuronal control of locomotion: from mollusc to man. Oxford University Press, Oxford

    Google Scholar 

  • Rybak IA, Shevtsova NA, Lafreniere-Roula M, McCrea DA (2006a) Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 577(2): 617–639

    Article  CAS  PubMed  Google Scholar 

  • Rybak IA, Stecina K, Shevtsova NA, McCrea DA (2006b) Modelling spinal circuitry involved in locomotor pattern generation: insights from the effects of afferent stimulation. J Physiol 577(2): 641–658

    Article  CAS  PubMed  Google Scholar 

  • Schomburg ED, Petersen N, Barajon I, Hultborn H (1998) Flexor reflex afferents reset the step cycle during fictive locomotion in the cat. Exp Brain Res 122(3): 339–350

    Article  CAS  PubMed  Google Scholar 

  • Shik ML, Orlovsky GN (1976) Neurophysiology of locomotor automatism. Phsyiol Rev 56(3): 465–501

    CAS  Google Scholar 

  • Taga G (1995a) A model of the neuro-musculo-skeletal system for human locomotion I. Emergence of basic gait. Biol Cybern 73: 97–111

    Article  CAS  PubMed  Google Scholar 

  • Taga G (1995b) A model of the neuro-musculo-skeletal system for human locomotion II. - Real-time adaptability under various constraints. Biol Cybern 73: 113–121

    Article  CAS  PubMed  Google Scholar 

  • Taga G, Yamaguchi Y, Shimizu H (1991) Self-organized control of bipedal locomotion by neural oscillators in unpredictable environment. Biol Cybern 65: 147–159

    Article  CAS  PubMed  Google Scholar 

  • Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93: 609–613

    Article  PubMed  Google Scholar 

  • Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5: 1226–1235

    Article  CAS  PubMed  Google Scholar 

  • Wadden T, Ekeberg Ö. (1998) A neuro-mechanical model of legged locomotion: single leg control. Biol Cybern 79: 161–173

    Article  CAS  PubMed  Google Scholar 

  • Whelan PJ, Hiebert GW, Pearson KG (1995) Stimulation of the group I extensor afferents prolongs the stance phase in walking cats. Brain Res 103: 20–30

    CAS  Google Scholar 

  • Winter DA (2004) Biomechanics and motor control of human movement, 3rd edn. Wiley, New York

    Google Scholar 

  • Yakovenko S, Gritsenko V, Prochazka A (2004) Contribution of stretch reflexes to locomotor control: a modeling study. Biol Cybern 90: 146–155

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki T, Nomura T, Sato S (2003a) Phase reset and dynamic stability during human gait. BioSystems 71: 221–232

    Article  PubMed  Google Scholar 

  • Yamasaki T, Nomura T, Sato S (2003b) Possible functional roles of phase resetting during walking. Biol Cybern 88: 468–496

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Aeronautics and Astronautics, Graduate School of Engineering, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto, 606-8501, Japan

    Shinya Aoi

  2. JST, CREST, 5 Sanbancho, Chiyoda-ku, Tokyo, 102-0075, Japan

    Shinya Aoi & Kazuo Tsuchiya

  3. Department of Mechanical Engineering, Faculty of Science and Technology, Keio University, 3-14-1 Hiyoshi, Kohoku-ku, Yokohama, 223-8522, Japan

    Naomichi Ogihara

  4. Department of Mechanical Engineering and Science, Graduate School of Engineering, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto, 606-8501, Japan

    Tetsuro Funato

  5. Deparment of Mechanical Engineering, Graduate School of Engineering, Osaka University, Yamadaoka 2-1, Suita, Osaka, 565-0871, Japan

    Yasuhiro Sugimoto

  6. Department of Energy and Mechanical Engineering, Faculty of Science and Engineering, Doshisha University, 1-3 Tatara, Miyakodani, Kyotanabe, Kyoto, 610-0394, Japan

    Kazuo Tsuchiya

Authors
  1. Shinya Aoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naomichi Ogihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tetsuro Funato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yasuhiro Sugimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kazuo Tsuchiya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shinya Aoi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aoi, S., Ogihara, N., Funato, T. et al. Evaluating functional roles of phase resetting in generation of adaptive human bipedal walking with a physiologically based model of the spinal pattern generator. Biol Cybern 102, 373–387 (2010). https://doi.org/10.1007/s00422-010-0373-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-010-0373-y

Keywords

Search

Navigation