Abstract
Reflexes are exquisitely sensitive to the motor task that is being performed at the time they are evoked; in other words, they are “task-dependent”. The purpose of this study was to investigate the extent to which the pattern of reflex modulation is conserved across three locomotor tasks that differ in muscle activity, joint kinematics, and stability demands. Subjects performed continuous level and incline walking on a treadmill and stair climbing on a stepping mill. Cutaneous reflexes were evoked by delivering trains of electrical stimulation to the sural nerve at the ankle at an intensity of two times the radiating threshold. Electromyographic (EMG) recordings were collected continuously from muscles in the arms, legs and trunk. Results showed that middle-latency reflex modulation patterns were generally conserved across the three locomotor tasks with a few notable exceptions related to specific functional requirements. For example, a reflex reversal was observed for tibialis anterior during stair climbing, which may be indicative of a specific adaptation to the task constraints. Overall our data suggest that the underlying neural mechanisms involved in coordinating level walking can be modified to also coordinate other locomotor tasks such as incline walking and stair climbing. Therefore, there may be considerable overlap in the neural control of different forms of locomotion.
Similar content being viewed by others
References
Andriacchi TP, Andersson GB, Fermier RW, Stern D, Galante JO (1980) A study of lower-limb mechanics during stair-climbing. J Bone Joint Surg Am 62:749–757
Baken BC, Dietz V, Duysens J (2005) Phase-dependent modulation of short latency cutaneous reflexes during walking in man. Brain Res 1031:268–275
Brooke JD, Cheng J, Collins DF, McIlroy WE, Misiaszek JE, Staines WR (1997) Sensori-sensory afferent conditioning with leg movement: gain control in spinal reflex and ascending paths. Prog Neurobiol 51:393–421
Burke RE, Jankowska E, Bruggencate GT (1970) A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae. J Physiol (Lond) 207:709–732
Burke D, Dickson HG, Skuse NF (1991) Task-dependent changes in the responses to low-threshold cutaneous afferent volleys in the human lower limb. J Physiol (Lond) 432:445–458
De Serres SJ, Yang JF, Patrick SK (1995) Mechanism for reflex reversal during walking in human tibialis anterior muscle revealed by single motor unit recording. J Physiol (Lond) 488:249–258
Duysens J, Trippel M, Horstmann GA, Dietz V (1990) Gating and reversal of reflexes in ankle muscles during human walking. Exp Brain Res 82:351–358
Duysens J, Tax AA, Trippel M, Dietz V (1993) Increased amplitude of cutaneous reflexes during human running as compared to standing. Brain Res 613:230–238
Duysens J, Tax AA, Murrer L, Dietz V (1996) Backward and forward walking use different patterns of phase-dependent modulation of cutaneous reflexes in humans. J Neurophysiol 76:301–310
Duysens J, Bastiannse CM, Smits-Engelsman BCM, Dietz V (2004) Gait acts as a gate for reflexes from the foot. Can J Physiol Pharmacol 82:715–722
Haridas C, Zehr EP (2003) Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol 90:2850–2861
Haridas C, Zehr EP, Misiaszek JE (2005) Postural uncertainty leads to dynamic control of cutaneous reflexes from the foot during human walking. Brain Res 1062:48–62
Hundza SR, Zehr EP (2006) Cutaneous reflexes during rhythmic arm cycling are insensitive to asymmetrical changes in crank length. Exp Brain Res 168:165–177
Jakobsson F, Borg K, Edstrom L, Grimby L (1988) Use of motor units in relation to muscle fiber type and size in man. Muscle Nerve 11:1211–1218
Kanda K, Sato H (1983) Reflex responses of human thigh muscles to non-noxious sural stimulation during stepping. Brain Res 288:378–380
Kanda K, Burke RE, Walmsley B (1977) Differential control of fast and slow twitch motor units in the decerebrate cat. Exp Brain Res 29:57–74
Komiyama T, Zehr EP, Stein RB (2000) Absence of nerve-specificity in human cutaneous reflexes during standing. Exp Brain Res 133:267–272
Laubenthal KN, Smidt GL, Kettelkamp DB (1972) A quantitative analysis of knee motion during activities of daily living. Phys Ther 52:34–43
Leroux A, Fung J, Barbeau H (1999) Adaptation of the walking pattern to uphill walking in normal and spinal-cord injured subjects. Exp Brain Res 126:359–368
Livingston LA, Stevenson JM, Olney SJ (1991) Stairclimbing kinematics on stairs of differing dimensions. Arch Phys Med Rehabil 72:398–402
Matthews PBC (1986) Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol (Lond) 374:73–90
McFadyen BJ, Winter DA (1988) An integrated biomechanical analysis of normal stair ascent and descent. J Biomech 21:733–744
Misiaszek JE, Krauss EM (2005) Restricting arm use enhances compensatory reactions of leg muscles during walking. Exp Brain Res 161:474–485
Nielsen J, Kagamihara Y (1993) Differential projection of the sural nerve to early and late recruited human tibailis anterior motor units: change of recruitment gain. Acta Physiol Scand 147:385–401
Riener R, Rabuffetti M, Frigo C (2002) Stair ascent and descent at different inclinations. Gait Posture 15:32–44
Schillings AM, Van Wezel BM, Duysens J (1996) Mechanically induced stumbling during human treadmill walking. J Neurosci Methods 67:11–17
Schubert M, Curt A, Jensen L, Dietz V (1997) Corticospinal input in human gait: modulation of magnetically evoked motor responses. Exp Brain Res 115:234–246
Simonsen EB, Dyhre-Poulsen P, Voigt M (1995) Excitability of the soleus H reflex during graded walking in humans. Acta Physiol Scand 153:21–32
Toft E, Sinkjaer T, Andreassen S, Larsen K (1991) Mechanical and electromyographic responses to stretch of the human ankle extensors. J Neurophysiol 65:1402–1410
Tokuhiro A, Nagashima H, Takechi H (1985) Electromyographic kinesiology of lower extremity muscles during slope walking. Arch Phys Med Rehabil 66:610–613
Van Wezel BM, Ottenhoff FA, Duysens J (1997) Dynamic control of location-specific information in tactile cutaneous reflexes from the foot during human walking. J Neurosci 17:3804–3814
Yang JY, Stein RB (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117
Zehr EP (2005) Neural control of rhythmic human movement: the common core hypothesis. Exerc Sport Sci Rev 33:54–60
Zehr EP, Hundza SR (2005) Forward and backward arm cycling are regulated by equivalent neural mechanisms. J Neurophysiol 93:633–640
Zehr EP, Stein RB (1999) What functions do reflexes serve during human locomotion? Prog Neurobiol 58:185–205
Zehr EP, Komiyama T, Stein RB (1997) Cutaneous reflexes during human gait: electromyographic and kinematic responses to electrical stimulation. J Neurophysiol 77:3311–3325
Zehr EP, Stein RB, Komiyama T (1998) Function of sural nerve reflexes during human walking. J Physiol (Lond) 507(Pt 1):305–314
Acknowledgments
The authors would like to thank Mr. A. Ley for excellent technical assistance and Dr. B.K.V. Maraj for helpful suggestions regarding experimental protocol and statistical analysis.
Author information
Authors and Affiliations
Corresponding author
Additional information
Grants: This work was supported by grants to EPZ from the Natural Sciences and Engineering Research Council of Canada (NSERC), the Michael Smith Foundation for Health Research, and the Heart and Stroke Foundation of Canada (BC & Yukon). EVL was supported in part by a Province of Alberta Graduate Scholarship.
Rights and permissions
About this article
Cite this article
Lamont, E.V., Zehr, E.P. Task-specific modulation of cutaneous reflexes expressed at functionally relevant gait cycle phases during level and incline walking and stair climbing. Exp Brain Res 173, 185–192 (2006). https://doi.org/10.1007/s00221-006-0586-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-006-0586-4