Summary
To investigate whether phase-dependent reversals in reflex responses on electromyography (EMG) are accompanied by movement reversals, a series of human volunteers were studied for their behavioural responses to sural nerve stimulation during running or walking on a treadmill. Low-intensity stimulation (< 2.5 x perception threshold, T) of the sural nerve yielded facilitatory responses in the tibialis anterior muscle (TA), correlated with an induced ankle dorsiflexion (mean maximum 4°) in early swing. The same stimuli yielded primarily TA suppression and weak ankle plantar flexion (mean maximum 1°) at end swing. The correlated induced knee angle changes did not precede the ankle changes, and they were relatively small. Mean maximum flexion in early swing was 6.2°, while mean maximum extension was 3.7°. High-intensity stimulation of the sural nerve (> 2.5 x T) always gave rise to suppression of the ongoing activity. This resulted in a second type of movement reversal. During late stance and early swing the responses in TA were suppressive (i.e. below background activity) and related to ankle plantar flexion. In contrast, the responses during early and middle stance consisted of suppression in extensor activity (gastrocnemius medialis and soleus) and ankle dorsiflexion.
The data are discussed in terms of a new hypothesis, which states that the responses to electrical stimulation of cutaneous nerves during locomotion do not correspond directly to corrections for stumbling following mechanical perturbations during the step cycle. Instead, the data invite a reinterpretation in terms of the opening and closing of reflex pathways, presumably by a central pattern generator for locomotion.
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References
Abraham LD, Marks WB, Loeb GE (1985) The distal hindlimb musculature of the cat. Exp Brain Res 58:594–603
Berger W, Dietz V, Quintern J (1984) Corrective reactions to stumbling in man: neuronal coordination of bilateral leg muscle activity during gait. J Physiol (Lond) 357:109–125
Creed RS, Denny-Brown D, Eccles JC, Liddell EGT, Sherrington CS (1932) Reflex activity of the spinal cord. Oxford University Press, Oxford
Dietz V, Quintern J, Berger W (1984) Corrective reactions to stumbling in man: functional significance of spinal and transcortical reflexes. Neurosci Lett 44:131–135
Dietz V, Quintern J, Berger W (1985) Afferent control of human stance and gait: evidence for blocking of group I afferents during gait. Exp Brain Res 61:153–163
Dietz V, Quintern J, Boos G, Berger W (1986a) Obstruction of the swing phase during gait: phase-dependent bilateral leg muscle coordination. Brain Res 384:166–169
Dietz V, Quinters J, Sillem M (1986b) Stumbling reactions in man: significance of proprioceptive and pre-programmed mechanisms. J Physiol (Lond) 386:149–163
Drew T, Rossignol S (1987) A kinematic and electromyographic study of cutaneous reflexes evoked from the forelimb of unrestrained walking cats. J Neurophysiol 57:1161–1184
Duysens J (1977) Reflex control of locomotion as revealed by stimulation of cutaneous afferents in spontaneously walking premammillary cats. J Neurophysiol 40:737–751
Duysens J (1981) A critique of the papers by Rossignol, Julien, Gauthier and Lund; Forssberg; Schomburg, Behrends and Steffens; and Andersson and Grillner. In: Taylor A and Prochazka (eds) Muscle receptors and movement. MacMillan, London, pp 433–436
Duysens J, Loeb GE (1980) Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats. J Neurophysiol 44:1024–1037
Duysens J and Pearson KG (1976) The role of cutaneous afferents from the distal hindlimb in the regulation of the step cycle of thalamic cats. Exp Brain Res 24:245–255
Duysens J and Stein RB (1978) Reflexes induced by nerve stimulation in walking cats with implanted cuff electrodes. Exp Brain Res 32:213–224
Duysens J, Loeb GE, Weston BJ (1980) Crossed flexor reflex responses and their reversal in freely walking cats. Brain Res 197:538–542
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 AAM, Doelen B van der, Trippel M, Dietz V (1991) Selective activation of human soleus or gastrocnemius in reflex responses during walking and running. Exp Brain Res 87:193–204
Eccles RM, Lundberg A (1959) Synaptic actions which may evoke the flexion reflex. Arch Ital Biol 97:199–221
Forssberg H (1979) Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. J Neurophysiol 42:936–953
Forssberg H, Grillner S, Rossignol S (1975) Phase dependent reflex reversal during walking in chronic spinal cats. Brain Res 85:103–107
Gollhofer A, Schmidtbleicher D, Quintern J, Dietz V (1986) Compensatory movements following gait perturbations: changes in cinematic and muscular activation patterns. Int J Sports Med 7:325–329
Loeb GE, Bak MJ and Duysens J (1977) Long-term unit recording from somato-sensory neurons in the spinal ganglia of the freely walking cat. Science 197:1192–1194
Loeb GE, Marks WB, Hoffer JA (1987) Cat hindlimb motoneurons during locomotion. IV. Participation in cutaneous reflexes. J Neurophysiol 57:563–573
Lundberg A, Malmgren K, Schomburg ED (1987) Reflex pathways from group II muscle afferents. 3. Secondary spindle afferents and the FRA: a new hypothesis. Exp Brain Res 65:294–300
McFayden BJ, Winter DA (1991) Anticipatory locomotor adjustments during obstructed human walking. Neurosci Res Commun 9 (1):37–45
Pratt CA, Chanaud CM, Loeb GE (1991) Functional complex muscles of the cat hindlimb. IV. Intramuscular distribution of movement command signals and cutaneous reflexes in broad, bifunctional thigh muscles. Exp Brain Res 85:281–299
Rossignol S, Drew T (1985) Interactions of segmental and suprasegmental inputs with the spinal pattern generator of locomotion. In: Barnes WJP, Gladden MH (eds) Feedback and motor control in invertebrates and vertebrates. Croom Helm, London, pp 355–377
Rossignol S, Drew T (1986) Phasic modulation of reflexes during rhythmic activity. In: Grillner S, Forssberg H, Stein PSG, Stuart D (eds) Neurobiology of vertebrate locomotion. MacMillan, London, pp 517–534 (Int Symp Series 45)
Rossignol S, Lund JP, Drew T (1988) The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates. In: Cohen A, Rossignol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York, pp 201–283
Wand P, Prochazka A, Sontag K-H (1980) Neuromuscular responses to gait perturbations in freely moving cats. Exp Brain Res 38:109–114
Yang JF and Stein RB (1988) Evidence for phase dependent cutaneous reflex reversal during walking in humans. Soc Neurosci 14:1303
Yang JF and Stein RB (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117
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Duysens, J., Tax, A.A.M., Trippel, M. et al. Phase-dependent reversal of reflexly induced movements during human gait. Exp Brain Res 90, 404–414 (1992). https://doi.org/10.1007/BF00227255
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DOI: https://doi.org/10.1007/BF00227255