PROPRIOCEPTION AND
LOCOMOTOR DISORDERS
Volker Dietz
Advances in our understanding of movement control allow us to define more precisely the
requirements for the rehabilitation of patients with movement disorders. Most purposeful,
complex movements are programmed in the central nervous system (CNS) and adapted by
proprioceptive feedback. The selection of and interaction between different sources of afferent
input is task dependent. Simple stretch reflexes are thought to be involved primarily in the control
of focal movement. For more complex motor behaviours such as locomotion, afferent input
related to load and hip-joint position probably has an important role in the proprioceptive
contribution to the activation pattern of the leg muscles. There is increasing evidence that
movement disorders such as spasticity and Parkinsons disease involve the defective use of
afferent input in combination with secondary compensatory processes. This has implications for
therapy, which should be directed to take advantage of the plasticity of the CNS.
CENTRAL PATTERN GENERATOR The study of movement control has relevance to our programming or reflex functioning. Rather, a move-
A neural circuit that produces general understanding of brain function. But it also has ment disorder also reflects secondary compensatory
self-sustaining patterns of implications for specific fields, such as neurology, processes that are induced by the primary lesion. In
behaviour independently of cognitive neuroscience, rehabilitation medicine and many cases, the altered motor behaviour can be consid-
sensory input.
robotics. Our understanding of movement disorders ered as the optimal outcome for a given lesion of the
and their appropriate treatment depends on knowledge motor system1. The complexity of primary and sec-
of the neuronal mechanisms that underlie functional ondary effects of a lesion means that detailed analysis of
movements. Movement disorders are the focus of one of a movement disorder is required to define the target
the most rapidly expanding fields in medicine, leading of any treatment.
to increasing costs of treatment and rehabilitation. This
review focuses on the role of proprioception during Basic aspects of locomotion
human locomotion, which can serve as a paradigm for It is generally accepted that locomotion in mammals
functional movements. depends on neuronal circuits (networks of interneu-
In a more general sense, locomotion is representative rons) in the spinal cord (the CENTRAL PATTERN GENERATOR,
of movement control. It is a subconsciously performed, or CPG) that can act in the absence of any afferent
everyday movement that is highly reproducible. It is input2. Afferent information influences the central
adapted automatically to existing conditions, such as (spinal) pattern and, conversely, the CPG selects appro-
ParaCare, Institute for ground irregularities, within a large safety margin. priate afferent information according to external
Rehabilitation and Research, Knowledge about the neuronal control of human loco- requirements2. In addition, proprioceptive information
University Hospital Balgrist, motion is also of broad interest for clinical reasons. provides the basis for a conscious representation of our
Forchstrasse 340, CH 8008, Characteristic disorders of locomotion are often the first body in space, which becomes severely disturbed in
Zurich, Switzerland.
e-mail:
sign of a central or peripheral lesion of the motor system. deafferented individuals3. Both the spinal locomotor
dietz@balgrist.unizh.ch However, impaired movement is not only the direct centre (CPG) and the reflexes that mediate afferent
doi:10.1038/nrn939 consequence of a central lesion, reflected in defective input to the spinal cord are under the control of the
brainstem4. In addition, there is phase-linked cortico- Control of body equilibrium. A basic aspect of the
spinal control of locomotion in humans57 and in other neuronal control of locomotion in both the quadru-
mammals8,9. Voluntary commands have to interact with pedal cat and the bipedal human concerns the
the spinal locomotor generator to change, for example, anti-gravity function of the leg extensors. It has been
the direction of gait or to avoid an obstacle10,11. For most suggested that the SPINAL STRETCH REFLEX adapts the pre-
other rhythmic elementary motor behaviours, such as programmed motor patterns of leg muscles to the ter-
hopping or swimming, CPGs are also assumed to exist2. rain, and compensates for unexpected changes in
Any disturbance of this finely coordinated interaction ground level18. Whereas this neuronal mechanism
between afferent inputs and pattern generation after a explains quick, unilateral patterns of reflex activity in
central lesion, such as stroke or spinal cord injury, leads leg extensor muscles, more complex bilateral coordi-
to a movement disorder. nation of leg muscle activation is needed to maintain
body equilibrium when gait is disturbed by an obsta-
Adequacy of animal models. The nature of motor- cle. Irrespective of the conditions under which stance
control mechanisms in humans can usually be deduced and gait are investigated, the neuronal pattern that is
only by indirect methods; such mechanisms are inferred evoked during a particular task is always directed to
from knowledge obtained from animal experiments. hold the bodys centre of mass over the base of support.
Consequently, it is not surprising that new treatments in All control mechanisms must therefore be considered
neurorehabilitation are frequently founded on basic and discussed in this respect. One consequence is that
research in quadrupeds12. For example, research on the selection of afferent input by central mechanisms
walking in cats has led to new therapies, such as loco- must correspond to the requirements for body stabi-
motor training for patients with spinal cord injuries13,14. lization. Neuronal signals of muscle stretch or length
For most of the basic mechanisms that underlie are insufficient for the control of bipedal posture.
locomotion, there seems to be no fundamental differ- Only a combination of afferent inputs can provide
ence between bipeds and quadrupeds1,15,16. Essential the information that is needed to control the bodys
spinal neuronal mechanisms, such as the afferent equilibrium during locomotion.
inputs that determine the locomotor pattern (includ-
ing hip-joint-related and load-receptor-related Interactions between afferent inputs. The control of
SPINALIZATION
Surgical separation of the spinal
inputs) are probably similar for quadrupedal and locomotion involves the use of afferent information
cord from the brain. bipedal locomotion. from a variety of sources in the visual, vestibular and
Nevertheless, there are also differences in the quanti- proprioceptive systems. As a rule, spinal reflex pathways
SPINAL STRETCH REFLEX tative relationships between central mechanisms and and descending pathways converge on common spinal
Also known as the short-latency
peripheral input. For example, the regulation of bipedal interneurons to integrate these inputs19. For example,
reflex, this is the simplest reflex
known. Muscle stretch is gait requires specific neuronal mechanisms to maintain visual feedforward information reduces the activity that
detected by muscle spindles, the the body in an upright position. Furthermore, the ability arises from the length sensors of muscles (the muscle
afferent (Ia) fibres of which of the isolated spinal cord to generate locomotor move- spindles)20. Furthermore, the amount of proprioceptive
monosynaptically (and ments is considerably greater in the SPINALIZED cat or rat7 feedback from the legs during various locomotor activi-
oligosynaptically) excite the
motor neurons that innervate
than in the monkey17 or in humans14. These differences ties determines the influence of vestibulospinal input on
the same muscle, leading to might be due to a greater dominance of supraspinal the stabilization of body movement21,22. Conversely,
muscle contraction. control over spinal neuronal circuits in humans. somatosensory loss increases vestibulospinal sensitivity 23.
DECEREBRATE adapt to irregularities of the ground. And third, the receptors in the sole of the foot, provides load informa-
Describes an animal in which activity of spinal polysynaptic reflexes depends on the tion63. The afferents that signal hip-joint position come
the spine and hindbrain have presence of contact forces, whereas flexor reflex mainly from muscles around the hip. The role of this
been isolated surgically from
responses can be elicited by tibial nerve stimulation afferent activity in rhythmic locomotion is to shape the
higher cortical inputs.
independently of loading57. pattern, to control phase transitions and to reinforce
Two main sources of afferent input are probably ongoing activity. Simple stretch and cutaneous reflexes
integrated in the polysynaptic reflex system: load-related might be involved in compensating for irregularities
and joint-position-related information. Load receptors, and in adapting to ground conditions.
or graviceptors, are thought to signal the influence of
gravity on the body to the spinal cord. There is only Load-related afferent input. A potentially excitatory
indirect evidence for such receptors in humans. For function of load receptors during locomotion was first
many years, the question of how the position of the described for the extensor muscles of the cat6466.
bodys centre of mass relative to the feet is signalled to Extensor load receptors are also suggested to provide
the CNS has been neglected in most studies of human essential information about the bodys centre of gravity
locomotion. To achieve appropriate gain control of pos- during locomotion in humans59,67,68. Experiments in the
tural reflexes, information is needed that signals the cat indicated that these receptor signals might arise
influence of gravity on the body. This information is from Golgi tendon organs and be carried by type Ib
insufficiently provided by muscle stretch receptors and afferents to the spinal locomotor generator.
the vestibular system. In humans, the influence of load receptors on the
regulation of stance and gait became evident from
Essential sources of proprioception studies of infant stepping67 and of weightlessness
During locomotion, multisensory proprioceptive feed- induced in adult humans either during space flight68 or
back is continuously weighted and selected. This process by water immersion59. Furthermore, it became clear
depends on the requirements of a particular locomotor that body load has an effect on the magnitude of the
task and the availability of afferent input. According to polysynaptic response, but not on the short-latency
observations made in healthy subjects59,60, small chil- stretch reflex in the gastrocnemius60,69,70. An influence
dren (BOX 1) and patients with paraplegia61,62, afferent of load-receptor input on vestibular-evoked postural
inputs from load receptors and hip joints make essential responses was also described recently for asymmetrical
contributions to the activation pattern of leg muscles standing71 (unequal distribution of body load on the
during human locomotion. two legs). It was suggested that there is a central inter-
It has been proposed that proprioceptive input from action between load-related afferent input from the
extensor muscles, and probably also from mechano- periphery and descending signals.
The effect of load-receptor input on leg extensor
activation during the stance phase of gait might be
Box 1 | Developmental aspects reinforced by heteronymous reflexes from ankle dorsi-
flexors72. One can assume that, during the stance phase
The innate pattern of locomotion, so-called newborn stepping, is characterized in of locomotion, type Ib afferents from extensors inhibit
humans, as in most of our mammalian ancestors, by digitigrade stepping (in which the the flexors64. This is functionally meaningful because
toes reach the ground first). This initial pattern of locomotion usually disappears after
the load on the stance limb must decrease before
a few weeks. At around nine months of age, a new phase begins, during which the child
swing can be initiated. In addition, extensor activity is
adapts the innate locomotor programme to the external conditions. These changes in
reinforced during the stance phase by positive feed-
leg muscle activity can be interpreted as a shift away from a low level of motor control
(with functionally ineffective monosynaptic stretch reflexes) towards patterns that are
back, which contributes to load compensation without
modulated by polysynaptic spinal reflexes89. This shift is biomechanically reflected in a leading to instability73,74.
stick-like usage of the legs in the early stage of stepping, whereas in older children, the
body rolls over the standing leg109,110. This maturation of the locomotor pattern can be Joint-position-related afferent input. In the cat, there
regarded as a process in which descending inhibition of monosynaptic (or early) are two main sources of afferent input that lead to
reflexes and facilitation of polysynaptic spinal reflexes are established. rhythm entrainment and/or resetting of locomotor
During infant stepping, the significance of load-receptor input to the locomotor activity. Such input can either block or induce a switch
pattern becomes clear62. Transient loading of infants during the stance phase of gait between the alternating flexor and extensor locomotor
produces an increase in ankle extensor electromyographic activity and a delay in bursts. The first of the afferent sources that satisfy these
tibialis anterior activity. In adults, loading leads only to increased extensor activity, but criteria is related to load, whereas the second is related
not to a delay in the flexor activity burst111. to hip position63,75,76. For example, a locomotor rhythm
Afferent input from the hip joints is also important for appropriate leg muscle can be entrained by using rhythmic hip movements in
activation in humans112,113, as it is in the cat75. If the hip is prevented from obtaining an spinalized77 and DECEREBRATE78 cats. The afferents that
extended position in small children, the generation of the flexor burst and the onset of signal hip-joint position come mainly from muscles
the swing phase are inhibited. that act around the hip. It has been suggested that
Human infants can generate coordinated bilateral muscle activation well before the receptors of the hairy skin can also provide high-
onset of independent walking. An initiation of the swing phase on one side is fidelity information about knee-joint movements
contingent on the contralateral limb being in the stance phase62,112,113. This is in humans79.
consistent with the interlimb coordination that is observed in the cat81,114,115 and in
In humans, observations made in infant stepping
adult humans52,53.
and in the isolated spinal cord of people with paraplegia
The impaired supraspinal control of spinal reflexes It is unclear how dysfunction of the basal ganglia
results in a loss of inhibition of short-latency reflexes, could affect load perception and loading responses
which leads to hyperexcitability of the simple stretch during gait. In this context, it is interesting to note
reflexes. This is combined with reduced facilitation of that the administration of levodopa (3,4-dihydroxy-
the functionally more important polysynaptic, or long- phenylalanine, or L-DOPA) or dopamine agonists is
latency, reflexes, which leads to a reduced proprioceptive associated with a depression of proprioception in
contribution to leg muscle activation during gait89. Parkinsons disease101.
Therefore, spastic gait is associated with reduced and The enhanced activation of the tibialis anterior dur-
less-well-modulated leg muscle activity. Consequently, ing the swing phase of gait in people with Parkinsons
the development of tension in leg extensor muscles dur- disease might reflect defective extensor suppression of
ing gait differs from that in healthy subjects and seems the flexor burst-generating circuitry74. The control
to be independent of exaggerated stretch reflexes (FIG. 3). of gait in these patients relies more on visual infor-
Furthermore, after a central motor lesion, the modula- mation and is exerted through modulation of leg
tion of both cutaneous90 and short-latency stretch91 flexor EMG activity79,102. This is in keeping with the
reflexes during the step cycle is impaired. As a conse- more general observation that visual information can
quence, the fast regulation of motor neuron discharge, substitute to some extent for the reduced proprio-
which characterizes normal muscle activation, is ception24. A strong dependency of people with
absent92,93. This contributes to the impairment of Parkinsons disease on visual cues during walking
walking ability in people with spasticity. becomes evident when an optical flow pattern is
Although muscle spasticity is neural in origin, there imposed during stepping on a treadmill 103. Whereas
is good evidence that spastic muscles are abnormal the walking velocity of healthy subjects is affected for
(FIG. 3). For example, reflex stiffness of ankle extensors only a short time by the pattern, people with
in people with spastic hemiparesis seems to be normal, Parkinsons disease continuously change their speed
but the intrinsic muscle stiffness is significantly higher with the movements of the optical flow.
than in control muscles91. Even the clinically assessed
muscle hypertonia in hemiparetic patients is found to Reliability of clinical tests
be associated primarily with muscle contracture and Neurorehabilitation is one of the most rapidly expand-
less with exaggerated reflexes94. In line with these ing fields in medicine, and this is leading to increasing
observations, recent studies indicate that spasticity costs of various forms of treatment. Only recently have
results in a major alteration of the normal musclejoint studies been conducted to address the effects of re-
anatomical relationship95. habilitation treatments on locomotion and functional-
Changes in the mechanical properties of muscle level outcomes, especially in people with hemiparesis
fibres can be attributed, at least in part, to muscle shorten- after stroke and with Parkinsons disease. Nevertheless,
ing. This might be the result of a decrease in the num- the assessment of isolated physical signs still prevails.
ber of sarcomeres along the myofibrils, accompanied Therefore, an important aim for the future is to establish
by increased resistance to stretch94. These observations standardized functional tests.
highlight the need to develop new rational treatment
procedures to replace the anti-spastic drugs that are Physical signs and function. Movement disorders are
frequently prescribed for mobile people with usually the first and most pronounced symptoms of an
spasticity 89. For example, by appropriate training pro- impairment in motor-centre function. The physical
grammes, compensatory processes could be guided in signs obtained during clinical examination, including
a preferable way. reflex excitability and muscle tone, can lead to a diagno-
In conclusion, after a central motor lesion, motor sis, but give little information about the pathophysiol-
units are transformed in such a way that regulation of ogy, course and appropriate treatment of a movement
muscle tone is achieved at a lower level of neuronal disorder. For example, stretch-reflex excitability and
organization, which in turn enables the patient to walk89. muscle tone differ fundamentally between the passive
Therefore, the altered regulation of spastic gait can be (clinical examination) and active (movement) condi-
considered as compensating for the loss of central tions. An appropriate treatment should not be cosmetic
motor-system function1. (that is, correcting an isolated clinical parameter that
does not affect function). For adequate therapy of a
Parkinsons disease. Several reports have indicated that movement disorder, it is essential to understand and
force control in Parkinsons disease is impaired during analyse the function of the reflexes and motor centres
both voluntary movements96,97 and locomotion98. that are involved, and their interaction with the bio-
Impaired load sensitivity develops with age and mechanical effector system in the motor task that is
becomes exaggerated in Parkinsons disease99. The con- impaired. Adapted behaviour emerges as an integration
sequence of such an impaired load-receptor mechanism of the biomechanical effector system and control
is a reduction in leg extensor activation that is proposed properties of the nervous system104.
to contribute to the gait disorder98,99 (FIG. 2b). A similar, This requires evaluation of the behaviour and func-
although opposite, change in threshold or bias has been tion of neuronal (EMG) and biomechanical (joint
described in cerebellar patients, who show hypermetric movement) measurements, as any changes in these sys-
postural responses during stance100. tems might lead to a movement disorder. Nevertheless,
Motor score
30
WISCI
treatment, either drugs or physical therapy, has to be 10
assessed on the basis of function. 20
Motor score
There are three requirements for appropriate eval- Locomotor function 5
10
uation of a therapeutic effect on function: that the (WISCI)
spontaneous recovery of function be separated from 0 0
25 36 39 71 83 179
the effect of any therapy; that the intensity and dura- Days after SCI
tion of a particular physical therapy, which strongly b
influences its effect105, be determined; and that 50 20
patients functional impairments be made comparable
40
by the use of internationally standardized scores for 15
Motor score
classification. 30
WISCI
10
20
Appropriate assessment of function. Owing to the
5
exquisite task-dependent regulation of nervous- 10
system function (discussed earlier), clinical tests must be
0 0
functional and specific. At present, it is a common and 17 29 41 55 69 83 98 104
accepted approach to score isolated clinical measures, Days after SCI
such as reflex excitability, muscle tone or voluntary force c
50 20
of single muscles. For example, muscle tone and spasm
frequency can be assessed by the Ashworth scale and the 40
15
Penn spasm-frequency scale, respectively106. For people
Motor score
WISCI
30
with spinal cord injury, the American Spinal Injury 10
Association (ASIA) has developed a standardized 20
neurological assessment the ASIA classification of 5
10
motor and sensory deficits107. The question is, first,
whether such scoring systems can serve as a sensitive 0 0
156 196 226 230 240 268 307
outcome measure for new interventional therapies, and
Days after SCI
second, whether they can reflect the functional impair-
ment, which is the most important aspect in terms of Figure 4 | Data from three patients with incomplete
the patients quality of life. paraplegia after spinal cord injury. In three individual
patients (ac) undergoing locomotor training, there is a
Only recently has a score been developed that differential course of motor score, which reflects the ability to
relates to function. Locomotor ability has been classi- voluntarily contract selected muscles, and locomotor function
fied into 19 items108. An ongoing study indicates that a with respect to time. The motor score is assigned according to
close relationship between motor scores and locomo- American Spinal Injury Association standards, with a maximum
tor ability exists only in patients with moderately score of 50. The WISCI (walking index for spinal cord injury)
impaired motor function. Patients with a low motor score ranges from 0 (no walking ability) to 19 (full walking
ability). SCI, spinal cord injury.
score who undergo intensive locomotor training can
achieve improved locomotor function without a
change in motor score (FIG. 4 and V.D. et al., unpub-
lished observations). In these cases, relatively little vol- Conclusions
untary force in the leg muscles (reflected in the ASIA Effective rehabilitation after a central motor lesion
score) is required to acquire the ability to walk when depends on the following points. First, knowledge
functional training is given. about the neuronal mechanisms that are involved in
For the future, the effectiveness of any new interven- the normal movement, and about the interactions
tional therapy should be assessed by internationally between the central programme and afferent inputs. It
accepted functional scores for upper- and lower-limb is also necessary to take into account the possibility
movements in combination with motor scores of that a movement disorder is the consequence not only
selected limb muscles. Motor and sensory scores are of the primary motor lesion, but also of secondary
most likely to reflect a spontaneous recovery of func- processes that can be compensatory and should be
tion, as they depend on the integrity of corticospinal supported during rehabilitation. The aim of rehabilita-
connections. By contrast, improvement of locomotor tion should focus on an improvement of function by
function after spinal cord injury also reflects the plastic- taking advantage of the plasticity of neuronal centres,
ity of neuronal spinal centres below the level of the rather than being directed towards the correction of
lesion. With the combined assessment of voluntary isolated clinical signs, such as reflex excitability. Finally,
force and automatic function, the superiority of any to monitor the outcome and assess the effectiveness of
new interventional therapy on functional movements any interventional therapy, standardized functional
might reliably be assessed. tests should be established.
1. Latash, M. L. & Anson, J. G. What are normal movements 24. Pearson, K. G. Motor system. Curr. Opin. Neurobiol. 10, 52. Dietz, V., Horstmann, G. A. & Berger, W. Interlimb
in atypical populations? Behav. Brain Sci. 19, 55106 (1996). 649654 (2000). coordination of leg muscle activation during perturbation of
This paper addresses an important point concerning 25. Hoffmann, P. Die Eigenreflexe Menschlicher Muskeln stance in humans. J. Neurophysiol. 62, 680693 (1989).
the self-compensation of a motor deficit and the (Springer, Berlin, 1922). 53. Dietz, V. Human neuronal control of automatic functional
associated problem of how far it is useful 26. Capaday, C. & Stein, R. B. Difference in the amplitude of movements: interaction between central programs and
cosmetically to correct secondary changes, such as the human soleus H-reflex during walking and running. afferent input. Physiol. Rev. 72, 3369 (1992).
muscle tone. J. Physiol. (Lond.) 392, 513522 (1987). 54. Lundberg, A. Multisensory control of spinal reflex pathways.
2. Grillner, S. in Wenner-Gren International Symposium Series 27. Morin, C., Katz, R., Mazires, L. & Pierrot-Deseilligny, E. Prog. Brain Res. 50, 1228 (1979).
Vol. 45. Neurobiology of Vertebrate Locomotion (eds Comparison of soleus H-reflex facilitation at the onset of 55. Yang, J. F. & Stein, R. B. Phase-dependent reflex reversal in
Grillner, S., Stein, P. S. G., Stuart, D. G., Forssberg, F. & soleus contractions produced voluntarily and during the human leg muscles during walking. J. Neurophysiol. 63,
Herman, R. M.) 505512 (Macmillan, London, 1986). stance phase of human gait. Neurosci. Lett. 33, 4753 11091117 (1990).
3. Sanes, J. N., Mauritz, K.-H., Dalakas, M. C. & Evarts, E. V. (1982). 56. Berger, W., Horstmann, G. & Dietz, V. Tension development
Motor control in humans with large-fiber sensory 28. Matthews, P. B. C. Mammalian Muscle Receptors and Their and muscle activation in the leg during gait in spastic
neuropathy. Hum. Neurobiol. 4, 101114 (1985). Central Actions (Arnold, London, 1972). hemiparesis: the independence of muscle hypertonia and
This paper describes the changes in motor 29. Loeb, G. E. & Hoffer, J. A. Activity of spindle afferents from exaggerated stretch reflexes. J. Neurol. Neurosurg.
behaviour that are observed in deafferented people cat anterior thigh muscles. II. Effects of fusimotor blockade. Psychiatry 47, 10291033 (1984).
(who lack proprioceptive feedback information J. Neurophysiol. 54, 565577 (1985). 57. Hiersemenzel, L., Curt, A. & Dietz, V. From spinal shock to
during movement). 30. Lackner, J. R. & DiZio, P. A. Aspects of body self-calibration. spasticity. Neuronal adaptations to a spinal cord injury.
4. Jankowska, E. & Lundberg, A. Interneurones in the spinal Trends Cogn. Sci. 4, 279288 (2000). Neurology 54, 15741582 (2000).
cord. Trends Neurosci. 4, 230233 (1981). 31. Sinkjaer, T., Anderson, J. B. & Larsen, B. Soleus stretch 58. Bussel, B. et al. Myoclonus in a patient with spinal
5. Capaday, C., Lavoie, B. A., Barbeau, H., Schneider, C. & reflex modulation during gait in humans. J. Neurophysiol. transection. Possible involvement of the spinal stepping
Bonnard, M. Studies on the corticospinal control of human 75, 11121120 (1996). generator. Brain 11, 12351245 (1988).
walking. I. Responses to focal transcranial magnetic 32. Verschueren, S. M. P., Swinnen, S. P., Desloovere, K. & One of the first indications that the isolated human
stimulation of the motor cortex. J. Neurophysiol. 81, Duysens, J. Effects of tendon vibration on the spinal cord contains neuronal networks that can
129139 (1999). spatiotemporal characteristics of human locomotion. Exp. generate locomotor-like EMG activity.
6. Schubert, M., Curt, A., Colombo, G. & Berger, W. Voluntary Brain Res. 143, 231239 (2002). 59. Dietz, V., Horstmann, G. A., Trippel, M. & Gollhofer, A.
control of human gait: conditioning of magnetically evoked 33. Ivanenko, Y. P., Grasso, R. & Lacquantini, F. Influence of leg Human postural reflexes and gravity an underwater
motor responses in a precision stepping task. Exp. Brain muscle vibration on human walking. J. Neurophysiol. 84, simulation. Neurosci. Lett. 106, 350355 (1989).
Res. 126, 583588 (1999). 17371747 (2000). 60. Dietz, V., Gollhofer, A., Kleiber, M. & Trippel, M. Regulation of
7. Schubert, M., Curt, A., Jensen, L. & Dietz, V. Corticospinal 34. Duysens, J., Tax, A. A. M., Trippel, M. & Dietz, V. bipedal stance: dependence on load receptors. Exp. Brain
input in human gait: modulation of magnetically evoked Increased amplitude of cutaneous reflexes during human Res. 89, 229231 (1992).
motor responses. Exp. Brain Res. 115, 234246 (1997). running as compared to standing. Brain Res. 613, 230238 61. Harkema, S. J. et al. Human lumbosacral spinal cord
The first evidence of corticospinal control of human (1993). interprets loading during stepping. J. Neurophysiol. 77,
locomotor movement, restricted to tibialis anterior 35. Tax, A. A., van Wezel, B. M. H. & Dietz, V. Bipedal reflex 797811 (1997).
activity at distinct phases of the swing. coordination to tactile stimulation of the sural nerve during 62. Dietz, V., Mller, R. & Colombo, G. Locomotor activity in
8. Drew, T. Role of the motor cortex in the control of visually human running. J. Neurophysiol. 73, 19471964 (1995). spinal man: significance of afferent input from joint and load
triggered gait modifications. Can. J. Physiol. Pharmacol. 36. Komiyama, T., Zehr, E. P. & Stein, R. B. Absence of nerve receptors. Brain (in the press).
74, 426442 (1996). specificity in human cutaneous reflexes during standing. 63. Dietz, V. & Duysens, J. Significance of load receptor input
9. Leblond, H., Menard, A. & Gossard, J. P. Corticospinal Exp. Brain Res. 133, 267272 (2000). during locomotion: a review. Gait Posture 11, 102110
control of locomotor pathways generating extensor activities 37. Zehr, E. P., Hesketh, K. L. & Chua, R. Differential regulation (2000).
in the cat. Exp. Brain Res. 138, 173184 (2001). of cutaneous and H-reflexes during leg cycling in humans. 64. Duysens, J. & Pearson, K. G. Inhibition of flexor burst
10. Bosco, G. & Poppele, R. E. Proprioception from a J. Neurophysiol. 85, 11781184 (2001). generation by loading extensor muscles in walking cats.
spinocerebellar perspective. Physiol. Rev. 81, 539568 38. Bastiaanse, C. M., Duysens, J. & Dietz, V. Modulation of Brain Res. 187, 321332 (1980).
(2001). cutaneous reflexes by load receptor input during human The first demonstration that loading strongly
11. Dietz, V. Neurophysiology of gait disorders: present and walking. Exp. Brain Res. 135, 189198 (2000). influences locomotor activity in the walking cat.
future applications. Electroencephalogr. Clin. Neurophysiol. 39. Zehr, E. P. & Stein, R. B. What functions do reflexes serve 65. Conway, B. A., Hultborn, H. & Kiehn, O. Proprioceptive input
103, 333355 (1997). during human locomotion? Prog. Neurobiol. 5, 185205 resets central locomotor rhythm in the spinal cat. Exp. Brain
12. Taub, E., Gitendra, U. & Elbert, T. New treatments in (1999). Res. 68, 643656 (1987).
neurorehabilitation founded on basic research. Nature Rev. 40. van Wezel, B. M., Ottenhoff, F. A. & Duysens, J. Dynamic 66. Pearson, K. G. & Collins, D. F. Reversal of the influence
Neurosci. 3, 228236 (2002). control of location-specific information in tactile cutaneous of group Ib-afferents from plantaris on activity in medial
13. Barbeau, H. & Fung, J. The role of rehabilitation in the reflexes from the foot during human walking. J. Neurosci. gastrocnemius muscle during locomotor activity.
recovery of walking in the neurological population. Curr. 17, 38043814 (1997). J. Neurophysiol. 70, 10091017 (1993)
Opin. Neurol. 14, 735740 (2001). 41. Zehr, E. P., Stein, R. B. & Komiyama, T. Function of sural 67. Yang, J. F., Stephens, M. J. & Vishram, R. Transient
14. Dietz, V., Colombo, G., Jensen, L. & Baumgartner, L. nerve reflexes during human walking. J. Physiol. (Lond.) disturbances to one limb produce coordinated, bilateral
Locomotor capacity of spinal cord in paraplegic patients. 507, 305314 (1998). responses during infant stepping. J. Neurophysiol. 79,
Ann. Neurol. 37, 574582 (1995). 42. Duysens, J. & van de Crommert, H. W. A. A. Neural control 23292337 (1998).
15. Macpherson, J. M., Horak, F. B., Dunbar, C. D. C. & Dow, of locomotion. Part 1: the central pattern generator from 68. Clement, G., Gurfinkel, V. S., Lestienne, F., Lipshits, M. J. &
R. S. Stance dependence on automatic postural cats to humans. Gait Posture 7, 131141 (1998). Popov, K. E. Changes of posture during transient
adjustments in humans. Exp. Brain Res. 78, 557566 (1989). 43. Brooke, J. D. et al. Sensori-sensory afferent conditioning perturbations in microgravity. Aviat. Space Environ. Med. 56,
16. Nilsson, J. A., Thorstensson, A. & Halbertsma, J. Changes with leg movement: gain control in spinal reflex and 666671 (1985).
in leg movements and muscle activity with speed of ascending paths. Prog. Neurobiol. 51, 393421 (1997). 69. Fouad, K., Bastiaanse, C. M. & Dietz, V. Reflex adaptations
locomotion and mode of progression in humans. Acta 44. Drew, T. & Rossignol, S. A kinematic and electromyographic during treadmill walking with increased body load. Exp.
Physiol. Scand. 123, 457475 (1985). study of cutaneous reflexes evoked from the forelimb of Brain Res. 137, 133140 (2001).
17. Vilensky, J. A. Locomotor behaviour and control in human unrestrained walking cats. J. Neurophysiol. 57, 11601184 70. Sinkjaer, T., Andersen, J. B., Ladoucoer, M., Christensen,
and non-human primates: comparison with cats and dogs. (1987). L. O. D. & Nielsen, J. B. Major role for sensory feedback in
Neurosci. Biobehav. Rev. 11, 263274 (1987). 45. Berger, W., Dietz, V. & Quintern, J. Corrective reactions to soleus EMG activity in the stance phase of walking in man.
18. Dietz, V., Quintern, J. & Sillem, M. Stumbling reactions in stumbling in man: neuronal co-ordination of bilateral leg J. Physiol. (Lond.) 523, 817827 (2000).
man: significance of proprioceptive and pre-programmed muscle activity during gait. J. Physiol. (Lond.) 357, 109125 71. Marsden, J. F., Castellote, J. & Day, B. L. Bipedal distribution
mechanisms. J. Physiol. (Lond.) 386, 149163 (1987). (1984). of human vestibular-evoked postural responses during
19. Schomburg, E. D. Spinal sensory systems and their 46. Lundberg, A., Malmgren, K. & Schomburg, E. D. Reflex asymmetrical standing. J. Physiol. (Lond.) 542, 323331
supraspinal control. Neurosci. Res. 7, 265340 (1990). pathway from group II muscle afferents. 3. Secondary (2002).
20. Jones, K. E., Wessberg, J. & Vallbo, A. Proprioceptive spindle afferents and the FRA: a new hypothesis. Exp. Brain 72. Marchand-Pauvert, V. & Nielsen, J. B. Modulation of
feedback is reduced during adaptation to a visuomotor Res. 65, 294306 (1987). heteronymous reflexes from ankle dorsiflexors to hamstring
transformation: preliminary findings. Neuroreport 12, 47. Nardone, A., Grasso, M., Giordano, A. & Schiepatti, M. muscles during human walking. Exp. Brain Res. 142,
40294033 (2001). Different effect of height on latency of leg and foot short- and 402408 (2002).
21. Brandt, T., Strupp, M. & Benson, J. You are better off medium-latency EMG responses to perturbation of stance 73. Prochazka, A., Gillard, D. & Bennet, D. J. Positive force
running than walking with acute vestibulopathy. Lancet 35, in humans. Neurosci. Lett. 206, 8992 (1996). feedback control of muscles. J. Neurophysiol. 77,
746 (1999). 48. Hasan, Z. & Stuart, D. G. Animal solutions to problems of 32263236 (1997).
This study provided the first evidence that the movement control: the role of proprioceptors. Annu. Rev. 74. Prochazka, A., Gillard, D. & Bennett, D. J. Indications
influence of vestibulospinal drive depends on the Neurosci. 1, 199223 (1988). of positive feedback in the control of movement.
speed of locomotion. 49. Hansen, P. D., Woollacott, M. H. & Debu, B. Postural J. Neurophysiol. 77, 3751 (1997).
22. Dietz, V., Baaken, B. & Colombo, G. Proprioceptive input responses to changing task conditions. Exp. Brain Res. References 73 and 74 provide convincing evidence
overrides vestibulo-spinal drive during human locomotion. 73, 627636 (1988). for movement control by positive force feedback
Neuroreport 12, 27432746 (2001). 50. Duysens, J., Trippel, M., Horstmann, G. A. & Dietz, V. Gating in the cat.
23. Horak, F. B. & Hlavacka, F. Somatosensory loss increases and reversal of reflexes in ankle muscles during human 75. Pearson, K. G. Proprioceptive regulation of locomotion.
vestibulospinal sensitivity. J. Neurophysiol. 86, 575585 walking. Exp. Brain Res. 82, 351358 (1990). Curr. Opin. Neurobiol. 5, 786791 (1995).
(2001). 51. Duysens, J., Tax, A. A. M., Murrer, L. & Dietz, V. Backward 76. Whelan, P. Control of locomotion in the decerebrate cat.
This study provided evidence of automatic and forward walking use different patterns of phase- Prog. Neurobiol. 49, 481515 (1996).
compensation of impaired proprioception by other dependent modulation of cutaneous reflexes in humans. 77. Andersson, O. & Grillner, S. Peripheral control of the cats
balance-regulating systems. J. Neurophysiol. 76, 301310 (1996). step cycle. II. Entrainment of the central pattern generators
for locomotion by sinusoidal hip movements during fictive 93. Rosenfalck, A. & Andreassen, S. Impaired regulation of force 108. Ditunno, J. F. et al. Walking index for spinal cord injury
locomotion. Acta Physiol. Scand. 118, 229239 (1983). and firing pattern of single motor units in patients with (WISCI): an international multicenter validity and reliability
78. Kriellaars, D. J., Brownstone, R. M., Noga, B. R. & spasticity. J. Neurol. Neurosurg. Psychiatry 43, 907916 study. Spinal Cord 38, 234243 (2000).
Jordan, L. M. Mechanical entrainment of fictive locomotion (1980). 109. Berger, W., Altenmller, E. & Dietz, V. Normal and impaired
in the decerebrate cat. J. Neurophysiol. 71, 20742086 94. ODwyer, N. J., Ada, L. & Neilson, P. D. Spasticity and development of childrens gait. Hum. Neurobiol. 3, 163170
(1994). muscle contracture following stroke. Brain 119, 17371749 (1984).
79. Edin, B. Cutaneous afferents provide information about knee (1996). 110. Sutherland, D. H., Olshen, R., Cooper, L. & Woo, S. L. Y.
joint movements in humans. J. Physiol. (Lond.) 531, This paper provided clear evidence that increased The development of mature gait. J. Bone Joint Surg. 62,
289297 (2001). muscle tone in spastic hemiparesis is due, in large 336353 (1980).
80. Iles, J. F. & Roberts, R. C. Inhibition of monosynaptic reflexes part, to muscle contracture. 111. Stephens, M. J. & Yang, J. F. Loading during the stance
in the human lower limb. J. Physiol. (Lond.) 385, 6987 95. Lieber, R. L. & Frieden, J. Spasticity causes a fundamental phase of walking in humans increases the extensor EMG
(1987). rearrangement of musclejoint interaction. Muscle Nerve 25, amplitude, but does not change the duration of step cycle.
81. Brower, B. & Ashby, P. Corticospinal projections to lower 265270 (2002). Exp. Brain Res. 12, 363370 (1999).
limb motoneurons in man. Exp. Brain Res. 89, 649654 96. Delwaide, P. J., Pepin, J. L. & Maertens de Noordhout, A. 112. Pang, M. Y. & Yang, J. F. The initiation of the swing phase in
(1992). Short-latency autogenic inhibition in patients with human infant stepping: importance of hip position and leg
This paper provided a physiological basis for the parkinsonian rigidity. Ann. Neurol. 30, 8389 (1991). loading. J. Physiol. (Lond.) 528, 389404 (2000).
differential neuronal control of lower-limb muscles. 97. Stelmach, G. E. in Tutorials in Motor Neuroscience (eds This study provided the first evidence in children of
82. Loeb, G. E. The control and responses of mammalian Requin, J. & Stelmach, G. E.) 137148 (Kluwer, Dordrecht, the significance of hip position and load-receptor
muscle spindles during normally executed tasks. Exerc. The Netherlands, 1991). input to the locomotor pattern.
Sport Sci. Rev. 12, 157204 (1984). 98. Dietz, V., Zijlstra, W., Prokop, T. & Berger, W. Leg muscle 113. Pang, M. Y. & Yang, J. F. Interlimb co-ordination in human
83. Hiebert, G. W. et al. Contribution of hind limb flexor muscle activation during gait in Parkinsons disease: adaptation and infant stepping. J. Physiol. (Lond.) 53, 617625 (2001).
afferents to the timing of phase transitions in the cat step interlimb coordination. Electroencephalogr. Clin. 114. Gorassini, M. A., Prochazka, A., Hiebert, G. W. & Gauthier,
cycle. J. Neurophysiol. 75, 11261137 (1996). Neurophysiol. 97, 408415 (1995). M. J. A. Corrective responses to loss of ground support
84. Dietz, V., Horstmann, G. A. & Berger, W. Perturbations of 99. Dietz, V. & Colombo, G. Influence of body load on the gait during walking. I. Intact cats. J. Neurophysiol. 71, 603610
human posture: influence of impulse modality on EMG pattern in Parkinsons disease. Mov. Disord. 13, 255261 (1994).
responses and cerebral evoked potential. J. Motor Behav. (1998). 115. Schomburg, E. D., Petersen, N., Barajon, I. & Hultborn, H.
21, 357372 (1989). 100. Horak, F. B. & Diener, H. C. Cerebellar control of postural Flexor reflex afferents reset the step cycle during fictive
85. Beloozerova, I. N. & Sirota, M. G. in Stance and Motor, scaling and central set in stance. J. Neurophysiol. 72, locomotion in the cat. Exp. Brain Res. 122, 339350 (1998).
Facts and Concepts (eds Gurfinkel, V. S., Joffe, M. E., 479486 (1994).
Massion, J. & Roll, J. P.) 163176 (Plenum, New York, 101. OSuilleabhain, P., Bullard, J. & Dewey, R. B. Proprioception Acknowledgements
1988). in Parkinsons disease is acutely depressed by I thank B. Ghwiler for helpful comments and R. Jurd for correcting
86. Calancie, B. et al. Voluntary stepping after chronic spinal dopaminergic medications. J. Neurol. Neurosurg. Psychiatry the English. The Swiss National Science Foundation and the
cord injury. Evidence for a central rhythm generator for 71, 607610 (2001). International Research Institute of Paraplegia supported this work.
locomotion in man. Brain 117, 11431159 (1994). 102. Dietz, V., Schubert, M. & Trippel, M. Visually-induced
87. Dobkin, B. H., Harkema, S., Requejo, P. & Edgerton, V. R. destabilization of human stance: neuronal control of leg
Modulation of motor-like EMG activity in subjects with muscles. Neuroreport 3, 449452 (1992). Online links
complete and incomplete spinal cord injury. J. Neurol. 103. Prokop, T. & Berger, W. Influence of optic flow on locomotion
Rehabil. 9, 183190 (1995). in normal subjects and patients with Parkinsons disease. DATABASES
88. Wirz, M., Colombo, G. & Dietz, V. Long term effects of Electroencephalogr. Clin. Neurophysiol. 99, 402 (1996). The following terms in this article are linked online to:
locomotor training in spinal man. J. Neurol. Neurosurg. 104. Taga, G. A model of the neuro-musculo-skeletal system for OMIM: http://www.ncbi.nlm.nih.gov/Omim/
Psychiatry 71, 9396 (2001). human locomotion. II. Real-time adaptability under various Parkinsons disease
89. Dietz, V. Spinal cord lesion: effects and perspectives for constraints. Biol. Cybern. 73, 113121 (1995).
treatment. Neural Plast. 8, 8390 (2001). 105. Kwakkel, G., Wagenaar, R. C., Twisk, J. W. R., Lankhorst, G. FURTHER INFORMATION
90. Jones, C. A. & Yang, J. F. Reflex behavior during walking in J. & Koetsier, J. C. Intensity of leg and arm training after American Spinal Injury Association: http://www.asia-
incomplete spinal-cord-injured subjects. Exp. Neurol. 128, primary middle-cerebral-artery stroke: a randomised trial. spinalinjury.org/
239248 (1994). Lancet 354, 191196 (1999). Encyclopedia of Life Sciences: http://www.els.net/
91. Sinkjaer, T. & Magnussen, I. Passive intrinsic and reflex- 106. Priebe, M. M., Sherwoord, A. M., Thornby, J. I., Kharas, N. F. bipedalism | central pattern generators | locomotion |
mediated stiffness in the ankle extensors of hemiplegic & Markowski, J. Clinical assessment of spasticity in spinal motor system organization | nervous control of movement |
patients. Brain 117, 355363 (1994). cord injury: a multidimensional problem. Arch. Phys. Med. proprioceptive sensory feedback | spinal reflexes |
92. Dietz, V., Ketelsen, U. P., Berger, W. & Quintern, J. Motor unit Rehabil. 77, 713716 (1996). tetrapod walking and running
involvement in spastic paresis: relationship between leg 107. Maynard, F. M. et al. International standards for neurological Volker Dietzs lab:
muscle activation and histochemistry. J. Neurol. Sci. 75, and functional classification of spinal cord injury. Spinal Cord http://www.neuroscience.unizh.ch/e/groups/dietz00.htm
89103 (1986). 35, 266274 (1997). Access to this interactive links box is free online.