PII S0361-9230(01)00504-4
Continuous, bilateral Achilles’ tendon vibration is not
detrimental to human walk
Gre ´ goire Courtine,
1
Thierry Pozzo,
1
Brigitte Lucas
2
and Marco Schieppati
1,3
*
1
Groupe d’Analyse du Mouvement, Universite ´ de Bourgogne, Campus Universitaire, Dijon, France;
2
Groupe
d’E
´
tudes et de Recherche sur le Handicap (GERSH), Centre de Convalescence et de Re ´e ´ ducation, Universite ´
de Bourgogne, Dijon, France; and
3
Istituto di Fisiologia Umana, Universita ` degli Studi di Pavia and Fondazione
Salvatore Maugeri (IRCCS), Scientific Institute of Pavia, Pavia, Italy
[Received 25 November 2000; Revised 27 March 2001; Accepted 27 March 2001]
ABSTRACT: Sensory feedback from the moving limbs contrib-
utes to the regulation of animal and human locomotion. How-
ever, the question of the specific role of the various modalities
is still open. Further, functional loss of leg afferent fibres due to
peripheral neuropathy does not always lead to major alteration
in the gait pattern. In order to gain further insight on proprio-
ceptive control of human gait, we applied vibratory tendon
stimulation, known to recruit spindle primary afferent fibres, to
both triceps surae muscles during normal floor walk. This pro-
cedure would disturb organisation and execution of walking,
especially if spindles fire continuously and subjects are blind-
folded. Vibration induced significant, though minor, changes in
duration and length of stance and swing phase, and on speed of
walking and kinematics of lower limb segments. No effect was
induced on angular displacement of the ankle joint or trunk and
head kinematics. This paucity of effects was at variance with
the perception of the subjects, who reported illusion of leg
stiffness and gait imbalance. These findings would speak for a
selective gating of Ia input during locomotion and emphasise
the notion that the central nervous system can cope with an
unusual continuous input along the Ia fibres from a key muscle
like the soleus. © 2001 Elsevier Science Inc.
KEY WORDS: Modulation, Proprioception, Spindle Ia input, Calf
muscles, Achilles’ tendon vibration, Gait.
INTRODUCTION
Locomotion consists of cyclic events controlled by central pattern
generating networks (CPGs) located within the spinal cord. They
are under the continuous influence of descending signals and
peripheral input [1,23]. Proprioceptive sensory feedback from the
moving limbs has repeatedly been shown to play a significant role
in the regulation of the CPG activity and in the gait adaptations to
the ground. For instance, in the walking system of the cat, near the
end of stance, a sensory signal switches the motor command from
stance to swing [22]. In general, in many vertebrate and inverte-
brate motor systems, the transition from one to another phase of
movement is triggered by a phasic afferent signal [32]. A possible
role of muscle afferent feedback is to control the level of activity
in antigravity muscles during the stance phase [33]. Positive and
negative feedback pathways from proprioceptors contribute sub-
stantially to the generation of activity in extensor muscles during
stance in the cat [25]. This indicates that the sensory feedback
mediated by muscle afferent fibres is closely integrated into the
activity of the spinal networks generating the locomotion. How-
ever, one may note that investigations made on de-afferented cats
have underlined no major alteration of the basic gait pattern
[23,39].
There is evidence that a spinal stepping generator exists in
humans [7,16] and there is growing support for a role of sensory
feedback in normal human locomotion [14,15]. However, the
question of the specific implication of the various modalities in the
control of locomotion is still open. For example, damage of leg
afferent fibres due to peripheral neuropathy as in diabetes does not
led to major alteration in the gait pattern [11], whilst complete loss
of large afferent fibres as in ganglionopathy creates major walking
problems [10]. In order to get further insight into the role of
proprioceptive information on human gait control, we applied
vibratory stimulation to both triceps surae muscles during normal
walk. Vibration is known to adequately recruit muscle spindle
group Ia afferents [6,37]. The tendon vibration reflex can be
induced in the soleus muscle by the continuous vibratory stimu-
lation [40], as evidence that muscle receptors are indeed ade-
quately stimulated by the mechanical effects of vibration. Further,
the H reflex depression, occurring both during and after vibration,
indicates ongoing activation of the presynaptic inhibition onto
large spindle afferent fibres. In addition, when applied at around 70
Hz, vibration can lock the firing pattern of most Ia fibres to the
stimulation pattern, thereby partly occluding the spindle input
during the gait cycle.
Irrespective of the induced muscle activation and reflex mod-
ulation, several investigations have established that vibration pro-
duces illusory changes in joint position [17–19] or even complex
drawing illusions [38]. Oriented whole-body tilt can be induced in
standing human subjects by applying vibratory stimulation [17,
30]; the vibration-induced sway is then oriented according to the
muscles vibrated [29]. At the same time, subjects report a subjec-
tive feeling of whole-body displacement [36]. Vibration applied to
lateral neck muscles prior to walking disrupts steering of locomo-
* Address for correspondence: Marco Schieppati, Istituto di Fisiologia Umana, Universita ` degli Studi di Pavia, Via Forlanini 6, I-27100 Pavia, Italy. Fax:
+00-39-382-507664; E-mail: marco.schieppati@unipv.it
Brain Research Bulletin, Vol. 55, No. 1, pp. 107–115, 2001
Copyright © 2001 Elsevier Science Inc.
Printed in the USA. All rights reserved
0361-9230/01/$–see front matter
107