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The Regulation of Limb Stiffness in the Context of Locomotor Tasks

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Progress in Motor Control

Abstract

Locomotion on ramped surfaces requires modulation of both pattern-generating circuits and limb stiffness. To meet the mechanical demands of locomotion under these conditions, muscular activation patterns must correspond to the appropriate functions, whether the muscles are serving as force generators or brakes. Limb stiffness is a critical mechanical property that determines how the body interacts with the environment, and is regulated by both intrinsic and neural mechanisms. We have recently investigated how pattern generation, stiffness, and proprioceptive feedback are modulated in a task-specific way using the decerebrate cat preparation. Our results confirm previous research using intact animals that during level and upslope walking, hip and ankle extensors are recruited for propulsion during stance. During downslope walking, hip extensors are inhibited and hip flexors are recruited during stance to provide the needed braking action. Our new data further show that endpoint stiffness of the limb is correspondingly reduced for walking down a slope, and that the reduction in stiffness is likely due to an increase in inhibitory force feedback. Our results further suggest that a body orientation signal derived from vestibular and neck proprioceptive information is responsible for the required muscular activation patterns as well as a reduction in limb stiffness. This increased compliance is consistent with the function of the distal limb to cushion the impact during the braking action of the antigravity musculature.

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Notes

  1. 1.

    The term “state” refers to a given organization of synaptic interactions and active neuronal pathways. For example, during locomotion, pathways mediating excitatory force feedback become active, altering the state of the spinal cord.

References

  • Abelew TA, Miller MD, Cope TC, Nichols TR. 2000. Local loss of proprioception results in disruption of interjoint coordination during locomotion in the cat. J Neurophysiol 84:2709–2714.

    PubMed  CAS  Google Scholar 

  • Ahn AN, Full RJ. 2002. A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect. J Exp Biol 205:379–389.

    PubMed  CAS  Google Scholar 

  • Angel MJ, Guertin P, Jimenez I, McCrea DA. 1996. Group I extensor afferents evoke disynaptic EPSPs in cat hindlimb extensor motorneurones during fictive locomotion. J Physiol 494(Pt 3):851–861.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ashley MJ, Gryfe CI, Amies A. 1977. A longitudinal study of falls in an elderly population II. Some circumstances of falling. Age Ageing 6:211–220.

    Article  PubMed  CAS  Google Scholar 

  • Bonasera SJ, Nichols TR. 1994. Mechanical actions of heterogenic reflexes linking long toe flexors with ankle and knee extensors of the cat hindlimb. J Neurophysiol 71:1096–1110.

    PubMed  CAS  Google Scholar 

  • Bonasera SJ, Nichols TR. 1996. Mechanical actions of heterogenic reflexes among ankle stabilizers and their interactions with plantarflexors of the cat hindlimb. J Neurophysiol 75:2050–2070.

    PubMed  CAS  Google Scholar 

  • Boyle R, Pompeiano O. 1981. Responses of vestibulospinal neurons to neck and macular vestibular inputs in the presence or absence of the paleocerebellum. Ann NY Acad Sci 374:373–394.

    Article  PubMed  CAS  Google Scholar 

  • Brink EE, Suzuki I, Timerick SJ, Wilson VJ. 1985. Tonic neck reflex of the decerebrate cat: a role for propriospinal neurons. J Neurophysiol 54:978–987.

    PubMed  CAS  Google Scholar 

  • Carlson-Kuhta P, Trank TV, Smith JL. 1998. Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking. J Neurophysiol 79:1687–1701.

    PubMed  CAS  Google Scholar 

  • Cham R, Redfern M. 2002. Changes in gait when anticipating slippery floors. Gait Posture 15:159–171.

    Article  PubMed  Google Scholar 

  • Donelan JM, Pearson KG. 2004. Contribution of sensory feedback to ongoing ankle extensor activity during the stance phase of walking. Can J Physiol Pharmacol 82:589–598.

    Article  PubMed  CAS  Google Scholar 

  • Donelan JM, McVea DA, Pearson KG. 2009. Force regulation of ankle extensor muscle activity in freely walking cats. J Neurophysiol 101:360–371.

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Duysens J, Clarac F, Cruse H. 2000. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80:83–133.

    PubMed  CAS  Google Scholar 

  • Eccles JC, Eccles RM, Lundberg A. 1957. Synaptic actions on motoneurones caused by impulses in Golgi tendon organ afferents. J Physiol 138:227–252.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fowler EG, Gregor RJ, Hodgson JA, Roy RR. 1993. Relationship between ankle muscle and joint kinetics during the stance phase of locomotion in the cat. J Biomech 26:465–483.

    Article  PubMed  CAS  Google Scholar 

  • Goslow GE, Jr., Reinking RM, Stuart DG. 1973. The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141:1–41.

    Article  PubMed  Google Scholar 

  • Gottschall JS, Nichols TR. 2007. Head pitch affects muscle activity in the decerebrate cat hindlimb during walking. Exp Brain Res 182:131–135.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gottschall JS, Nichols TR. 2011. Neuromuscular strategies for the transitions between level and hill surfaces during walking. Philos Trans R Soc Lond B Biol Sci 366:1565–1579.

    Article  PubMed  PubMed Central  Google Scholar 

  • Granit R. 1950. Reflex self-regulation of muscle contraction and autogenetic inhibition. J Neurophysiol 13:351–372.

    PubMed  CAS  Google Scholar 

  • Gregor RJ, Smith DW, Prilutsky BI. 2006. Mechanics of slope walking in the cat: quantification of muscle load, length change, and ankle extensor EMG patterns. J Neurophysiol 95:1397–1409.

    Article  PubMed  Google Scholar 

  • Grillner S, Shik ML. 1973. On the descending control of the lumbosacral spinal cord from the “mesencephalic locomotor region”. Acta Physiol Scand 87:320–333.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Houk J. 1972. The phylogeny of muscular control configurations. In: Drischel P, Dettmar P, editors. Biocybernetics. Jena: Fisher. pp 125–144.

    Google Scholar 

  • Houk J, Crago P, Rymer W. 1981. Function of the spindle dynamic response in stiffness regulation - a predictive mechanism provided by nonlinear feedback. In: Taylor A, Prochazka A, editors. Muscle Receptors and Movement. London: Macmillan. pp 299–309.

    Google Scholar 

  • Huyghues-Despointes CM, Cope TC, Nichols TR. 2003. Intrinsic properties and reflex compensation in reinnervated triceps surae muscles of the cat: effect of movement history. J Neurophysiol 90:1547–1555.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lay A, Hass C, Gregor R. 2006. The effects of sloped surfaces on locomotion: a kinematic and kinetic analysis. J Biomech 39:1621–1628.

    Article  PubMed  Google Scholar 

  • Lay AN, Hass CJ, Gregor RJ. 2007. The effects of sloped surfaces on locomotion: backward walking as a perturbation. J Biomech 40:3050–3055.

    Article  PubMed  Google Scholar 

  • Lindsay KW, Roberts TD, Rosenberg JR. 1976. Asymmetric tonic labyrinth reflexes and their interaction with neck reflexes in the decerebrate cat. J Physiol 261:583–601.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Maas H, Prilutsky BI, Nichols TR, Gregor RJ. 2007. The effects of self-reinnervation of cat medial and lateral gastrocnemius muscles on hindlimb kinematics in slope walking. Exp Brain Res 181:377–393.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maas H, Gregor RJ, Hodson-Tole EF, Farrell BJ, English AW, Prilutsky BI. 2010. Locomotor changes in length and EMG activity of feline medial gastrocnemius muscle following paralysis of two synergists. Exp Brain Res 203:681–692.

    Article  PubMed  PubMed Central  Google Scholar 

  • Magnus R, de Kleijn A. 1912. Die Abhangigkeit des Tonus der Extremitatenmuskeln von der Kopfstellung. Pflugers Arch 145:455–548.

    Article  Google Scholar 

  • Manzoni D, Andre P, Pompeiano O. 2004. Proprioceptive neck influences modify the information about tilt direction coded by the cerebellar anterior vermis. Acta Otolaryngol 124:475–480.

    Article  PubMed  CAS  Google Scholar 

  • Marchand AR, Manzoni D, Pompeiano O, Stampacchia G. 1987. Effects of stimulation of vestibular and neck receptors on Deiters neurons projecting to the lumbosacral cord. Pflugers Arch 409:13–23.

    Article  PubMed  CAS  Google Scholar 

  • Nichols TR, Houk JC. 1976. Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol 39:119–142.

    PubMed  CAS  Google Scholar 

  • Nichols R, Ross KT. 2009. The implications of force feedback for the lambda model. Adv Exp Med Biol 629:663–679.

    Article  PubMed  Google Scholar 

  • Nichols TR, Cope TC, Abelew TA. 1999. Rapid spinal mechanisms of motor coordination. Exerc Sport Sci Rev 27:255–284.

    PubMed  CAS  Google Scholar 

  • Polcyn AF, Lipsitz LA, Kerrigan DC, Collins JJ. 1998. Age-related changes in the initiation of gait: degradation of central mechanisms for momentum generation. Arch Phys Med Rehabil 79:1582–1589.

    Article  PubMed  CAS  Google Scholar 

  • Prentice SD, Hasler EN, Groves JJ, Frank JS. 2004. Locomotor adaptations for changes in the slope of the walking surface. Gait Posture 20:255–265.

    Article  PubMed  Google Scholar 

  • Prilutsky BI, Maas H, Bulgakova M, Hodson-Tole EF, Gregor RJ. 2011. Short-term motor compensations to denervation of feline soleus and lateral gastrocnemius result in preservation of ankle mechanical output during locomotion. Cells Tissues Organs 193:310–324.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ross KT, Nichols TR. 2009. Heterogenic feedback between hindlimb extensors in the spontaneously locomoting premammillary cat. J Neurophysiol 101:184–197.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ross K, Duysens J, Smith V, Nichols T. 2005. Modulation of cutaneous and proprioceptive feedback in the premammillary locomoting cat. Soc Neurosci Abstr 30:630–637.

    Google Scholar 

  • Smith JL, Carlson-Kuhta P, Trank TV. 1998. Forms of forward quadrupedal locomotion. III. A comparison of posture, hindlimb kinematics, and motor patterns for downslope and level walking. J Neurophysiol 79:1702–1716.

    PubMed  CAS  Google Scholar 

  • Srivastava UC, Manzoni D, Pompeiano O, Stampacchia G. 1984. Responses of medullary reticulospinal neurons to sinusoidal rotation of neck in the decerebrate cat. Neuroscience 11:473–486.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki I, Timerick SJ, Wilson VJ. 1985. Body position with respect to the head or body position in space is coded by lumbar interneurons. J Neurophysiol 54:123–133.

    PubMed  CAS  Google Scholar 

  • Tinetti ME, Doucette J, Claus E, Marottoli R. 1995. Risk factors for serious injury during falls by older persons in the community. J Am Geriatr Soc 43:1214–1221.

    PubMed  CAS  Google Scholar 

  • Tuthill C, Nichols T. 2008. Context-dependent organization of force feedback in the decerebrate cat. Soc Neurosci Abstr 34:377–373.

    Google Scholar 

  • Tuthill C, Nichols TR. 2012. Task dependent changes to hindlimb impedance in the decerebrate cat. Soc Neurosci Abstr 38:886–811.

    Google Scholar 

  • von Holst E, Mittelstaedt H. 1950. Das reafferenzprincip. Naturwiss 47:464–476.

    Article  Google Scholar 

  • Wilmink RJ, Nichols TR. 2003. Distribution of heterogenic reflexes among the quadriceps and triceps surae muscles of the cat hind limb. J Neurophysiol 90:2310–2324.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants NS20855 and HD32571.

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Correspondence to T. Richard Nichols .

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Nichols, T., Gottschall, J., Tuthill, C. (2014). The Regulation of Limb Stiffness in the Context of Locomotor Tasks. In: Levin, M. (eds) Progress in Motor Control. Advances in Experimental Medicine and Biology, vol 826. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1338-1_4

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