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Normal gait is differentially influenced by the otoliths
Normal gait is differentially otoliths W.H. Zangemeister”, “‘Neurological University Fondazione Pro Juventute Received January
I!)9
I, accepted
M.V. Bulgheroni’.
influenced
and A. Pedotti’
Clinic, Hamburg, Germany; .‘Centro di Don C. Gnocchi e Politecnico di Milano, Italy May
by the
Bioengegneria,
I Ii!)1
ABSTRACT Postural control depends on the integration of vestibular, somatosensory and visual orientation signals. The otolith contribution topostural control is achieved by the integration of otolith inputs andperipheral afferent inputs involved in crossed reJex pathways. This study shows that a functional linkage between otolith signals and activity in lower limb muscles is detectable in normal human gait. The otolith input appears to dominate particularly the neck proprioceptive and gaze motor influences during normal gait. This is demonstrated by an increase of tibialis anterior muscle activi[y during retrojlexion of the head/neck, leading to an increased stability and counteracting possible perturbations. It is also shown by decrease of roordination during the movement caused b.v larger displacement of the centre of gravity demonstrated in vector dia
Gait analysis,
vestibular-neck-influence
on gait. kinematical-EMG-forceplate
INTRODUCTION When a human being experiences a change of posture, the vestibular system can only initiate appropriate body postural reflexes if the relative position between the labyrinths and the body is known. A continuous flow of information from neck proprioceptors and other position receptors of the vertebral column is thus essential for a proper functioning of the vestibular system. Such afferents interact with postural control circuits of the brain stem at various levels, including the vestibular nuclei, thereby not only gaining access to neuronal substrates which guide postural reflexes of the body but also to circuits mediating such reflexes of the oculomotor and gaze motor system. The vestibular system monitors the forces associated with angular and linear acceleration of the head by means of five organs located within the labyrinthine cavities of the temporal bones on each side of the skull. The saccular and urticular sense linear acceleration, and the cristae of the three semicircular canals sense angular acceleration of the head. The capacity of the maculae and cristae to function as sensors of linear and angular acceleration, respecconfiguration’. tively, rests on their anatomical When we reviewed the literature with respect to the influence of vertical head/eye posture on gait, most data referred to the otoliths’ influence on postural activities during stance. Clear information on their influence on gait, especially in humans, is lacking and in this study two questions were pursued. Correspondence and reprint requests to: Prof. Dr W.H. Zangemeister, Neurological University Clinic Hamburg-Eppendorf, Martinistr. 52, D 2000 Hamburg 20, Germany @ I!)!)1 Butterworth-Heinemann ol~l-s12T,/!~l/olio~lil-ox
analysis,
gaze-gait
control
When normal humans walk under three different conditions of vertical head posture, i.e. primary position, 45” anteflexion, 45” retroflexion, would it be ossible to distinguish for these subjects responses besides the general arousal effect of this manoeuvre) P that resemble clinical intuitive observations from patients with different kinds of spasticity as reported in the early literature”.” (Figure 7). Secondly, how could such results fit into recent observations on the linkage between gaze position, otolith influences and neck muscles as the upper most part of the truncal/ skeletal muscles”‘?
METHODS In order to develop a precise analysis of human gait under different conditions we used the ELITE system, a motion analyser (Figure 2). This system allows a multifactorial analysis of the walking cycle by means of simultaneous acquisition and processing of TV images and analogue signals from a force platform and an EMG unit. The core of the system is an image processor which analyses the frames coming from two TV cameras’“. It detects the presence and the position of passive markers worn by the subject in real time. The special algorithm of bi-dimensional crosscorrelation adopted in the ELITE system to detect the position of markers allows one to obtain a very high precision and accuracy. To quantify this accuracy, special tests were performed. They consisted of measuring the distance between spherical markers fixed to a rigid body in static and dynamic conditions. In the operative conditions two TV cameras were
for BES J. Biomed.
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Injluence of otolith
on gait: W.H. Zangemeister et al Labyrmth
Neck Head up
Dowflexed
Head down
Head narmal
T-f
b
a Normal
d
’
e
Ventnflexed
h
g
C
I
I
f
\
P-
Figure 1 Schema of combined effects on limbs produced by the positional reflexes from the neck and from the labyrinth (right lateral views) (both modified from ref. 3). Note that the row labelled neck normal, d, e, f, represents the normal otolith dominance with legs flexed/head up and legs extended/head down. The column headed head normal, b, e, h, represents the pathological condition of neck static dominance. This refers to Magnus’ and his results regarding neck reflexes in decerebrated mammals. Our experimental condition for bipedal gait with respect to the antigravity muscles would be depicted in d and f. The neck normal condition obviously has been sketched by Roberts’ in a simplified way for easy understanding of the concept. Of course, in most quadrupedal mammals the neck normal condition would refer to a head retroflexion of about Ii;“. In humans the neck normal condition applies to an approximately 15” anteflexion of the head
used (SD acquisition) and we obtained the following results. In the static condition (motionless object in different parts of the field of view) the average measurement precision of the marker position is one part on 19 750 and in the dynamic condition (object moving through the field of view) the average measurement precision of marker position is one part on 2800. During these experimental trials the two TV
cameras were placed at a distance of about 5m on one side of the walking pathway. They were 5 m away from each other and were placed at a height of about 1 m from the ground. Fifty frames per second were processed in real time by the ELITE system for each TV camera. The coordinates of the detected markers were sent to the host computer, a Digital PDPl l/73, where a second level processing took place. A complex tracking procedure allowed a completely automatic classification of the markers and the reconstruction of their trajectories even when some markers were temporarily hidden or their trajectories intersected’ ‘. After the classification of the markers recognized by each TV camera, the system performed the three dimensional reconstruction and the computing of linear velocities and accelerations for each marker and each frame. The ground reaction forces (GRF) were recorded by means of a Kistler force platform. The signals from the transducers were sent to a charge amplifier connected to the host computer. The sampling frequency of the data from the charge amplifier was FiOHz. The host computer processed the acquired data to compute the components of the ground reaction forces Fx, Fy and Fz and the progression of their application point on the platform surface. These results were globally represented as two vectograms which illustrate the space evolution of the ground reaction forces in the sagittal and in the frontal planel4 13. The myoelectric signals were recorded by means of a telemetric system composed by an EMG receiver and by a portable unit worn by the sub’ect that was directly connected to the surface electro d es placed on the muscular masses of interest. The bandpass of the EMG system used was 16-2.50Hz. The signals from the receiver were sampled by the host computer with
EMG receiver
Kinematical
TV
reports
camera TV camera 2 Force platform
1
processor
,
L] Dynamical
reports
Charge amplifier
EMG reports Figure 2 An overview of the ELITE system. The subject moves in the field of view of two TV cameras to allow a three dimensional analysis of his motion. He wears retroflective markers on the anatomical points of interest. The image processor recognizes these markers and sends their coordinates to the host computer for further elaborations. The subject also wears surface electrodes connected to a portable EMG transmitter. The myoelectric signals are filtered and amplified by the receiver and then sent to a computer. The signals coming from the force platform are preprocessed by the charge amplifier. The components of the ground reaction forces and their application points are then sent to the computer. After a second level processing, different reports of the measured data are ready for output
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Injkmce of otolith on guit: W.H. Zungemeisteret al.
a frequency of ,500 H z. The resolution of the A/D converter was 12 bits for all the 16 analogue signals (8 channels for ground reactions and 8 channels for myoelectric activities). During the experimental trials the subject wore 10 markers placed on cheek bone, jaw corner, shoulder, elbow, hip, trocanter, knee, ankle, heel and fifth metatarsal head of the right leg. The surface electrodes were placed on the vastus medialis (VM), biceps femoris (BF), tibialis anterior (TA) and gastrocnemius (GC) of the same leg. To prevent artifacts and electrical noise the electrodes were placed after cleaning, depilation and scraping of the skin. An analogue integrator provided the rectified and integated EMG signals while a simple resistances’ circuit placed under the shoe sole made it possible to reconstruct the phases of walking cycle that were also recorded on an X-channel UV recorder.
cadence. For each condition the subject performed at least IO trials. For comparison with quiet stance conditions, the subject was asked to stand for few seconds (30-60s) in each of the conditions described above while EMG and VDT were performed. Quantification of head posture was done by using the ELITE system. We examined five subjects who were 27 & 8 years old. They were all right-handed and, to guarantee homogeneous starting conditions, wore tennis shoes. For the analysis of the data we considered kinematic, dynamic and myoelectrical parameters. As far as kinematics are concerned we analysed trajectories, velocities and accelerations of all markers worn by the subject, particularly in the forward direction. Concerning dynamics we chose to focus on the progression of the application point and on the trend of the force path. The analysis of the myoelectrical activity was executed on the raw signal and on the rectified and integrated signal. By analogue instrumentation the signal was filtered in the range of ‘LO-250 Hz with an amplifier gain of 2500. Integration was obtained by analogue means as well with a time constant of .50 ms. After preprocessing the data in that fashion, we focused attention on the main myoelectric parameters such as amplitude, duration and latency of the most significant activity bursts.
Test procedure At the beginning the subject was asked to walk at a natural cadence for some steps in order to obtain ten recordings of gait in normal conditions, demonstrating the repeatability of gait parameters under normal conditions. The condition for the second set of trials was with head placed 45” down. In the third condition the subject walked with head placed 4.5” up. The last two sets of walking cycles were performed with the head turned X0” towards the right and left, respectively. In all these conditions there were no variations in gaze direction, i.e. the eyes were looking straight ahead, and walking
Normoi
RESULTS The kinematic analysis was based on the examination velocities and accelerations of all of trajectories, markers. Comparison between the quantitative kine-
Head down
wolkq
I
I
Heod up
7
Figure 3 Comparison of kinematic parameters in the conditions of normal walking, with head down and with head up. a, stick diagrams; b, X coordinates of leg markers; the measured length stride is reported in millimetres. (H, heel; M, lateral malleolus; Vm, F’th metatarsal head; K, knee; T, trochanter; Hi, hip, iliac crest. These last two markers are practically always superimposed. The same terminology applies to the subsequent three figures. c, Y coordinates of leg markers. The coordinates of the markers are measured in mm. The upper marker corresponds to the iliac crest, the second to the trochanter, the third to the knee, the fourth to the malleolus, the fifth to the Vth metatarsal head and the last to the heel
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matic data obtained for every single condition ensured a high repeatability of their trend. Figure 3 shows a stick diagram and trajectories of leg markers during three trials performed in normal conditions, with head down and with head up, respectively. The stick diagram clearly shows the different head posture in these three conditions. In the first column, where the condition of normal walking is depicted, it is possible to compute a reference value of inclination which defines the normal vertical position. This value is obtained by computing the angle between the segment linking the two head markers and the vertical direction. In the other rows of Figure 3 the X and Y coordinates of the leg markers in the three main conditions are compared. The X axis is coincident with the walking direction, while the Y axis is the vertical axis. In Figure 3b the trajectories of leg markers along the walking direction are depicted. The difference between the motion of the upper (hip and greater trochanter) markers and the motion of the lower ones (knee and foot markers) is evident. Upper markers show a linear trend (uniform velocity) while knee and foot markers show some oscillations around a straight line. With regard to the foot trajectories, it is easy to distinguish the stance phase, i.e. when the values for the X coordinates do not vary and the swing phase, when the same values increase almost linearly. In Figure 3c, the upper markers demonstrate a slight periodic vertical oscillation and a similar path, while the foot markers show larger height variations during the swing phase. The 2 coordinates are not illustrated because walking develops mainly on a straight line and displacements in the horizontal plane are not significant. There are practically no variations for all the coordinates. The same is also true for velocities and accelerations (Figure 4). In Figure 4a the velocities along the walking direcof the upper markers tion’ are shown. The velocit (hip and greater trochanter r is almost constant as suggested by the linear trajectories, while the foot markers show a velocity peak in the middle of the swing phase. Obviously their velocity becomes zero during stance phase. In the vertical direction (Figure 4b) the only significant variations of velocity are during the swing phase and even in this direction, the most typical behaviour is shown by the foot markers displaying three velocity peaks: two of them have positive values and take place at the beginning and at the end of the swing phase, while a negative one characterizes the middle of the swing phase. (Fi ure 4c,d), a With regard to head accelerations periodic trend in these directions (.Kand ys is evident. It was observed that the amplitude of the acceleration in the x direction was low for head up compared to head down, and increased in the y direction, respectively, for head up. In Figure 4c,d, the extrema and zero-crossings of x and y head accelerations appear to be about 180” out of phase. This was true for all conditions with only slight variations between down and up. Because the utricule is close to its optimum working range in the down position and, conversely, out of its working range in the up position a different compound linear acceleration vector would result, if the effect of
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L
a
b
Comparisonof kinematical parameters in the conditions of normal walking, with head down and with head up. a, Velocities in the X direction of leg markers; b, velocities in the Y direction of leg markers; c, acceleration in X direction of the upper head (cheekbone) marker; d, acceleration in the Y direction of the upper head (cheekbone) marker. The velocities of the markers are measured in mms ’ and the accelerations in mms ‘. Values of velocity and acceleration are represented by using a self-adjusting technique, so that each diaFam is scaled to its range of variation Figure 4
gravity is taken into account given similar acceleration dynamics for all conditions. Thus different otolith stimulations should result in a change of leg EMG activities. However, there were no variations even in stride length. The same results were obtained for head turning to the right and to the left. All respective results were reproducible in all subjects.
EMG analysis The analysis of the myoelectric recordings demonstrated distinct differences particularly in the head up condition (Figure 5). Normal condition. The comparison with torques at joints clarified the information content of the EMG, especially regarding the intersubject features and the sequence of muscle activation. Even with qualitative analysis of the EMG signals it appeared that, despite similar kinematics and speed, the EMG patterns of different subjects were in agreement with the respective torques computed by the mathematical model. This was in line with the results reported by Pedotti’ ‘. The main neuromuscular events beyond the normal expected statistical variation could be thus established in a precise way. Inaccuracies due to the recording procedure could also be reasonably excluded. Head up condition. With the head up all sub‘ects showed a significant increase of tibialis anterior iTA)
Figure 5 Comparison of EMG activittes in the conditions muscles and stride phases; b, typical rectified and integrated respectively
of normal recordings
activity (Table 7). In addition to a significant I b < w3.l 1) general increase of tonic activity of TA &ring the whole walking cycle, the most interesting phenomenon was the appearance of a third activity burst in the middle of the stance phase. The amplitude of such a burst ranged from 1.1 to 2..5 mV and its duration from 90 to 320ms. This phenomenon was, in general, present in the recordings of all subjects. This was not seen under other conditions. A nonparametric statistical analysis (Table 7, Wilcoxon test’“) on the probability of the appearance of such a third burst demonstrated that under normal conditions it occurred in 32% of cases. However, in the head up condition, it occurred in 80% of cases, with head down in 23%) of cases. This difference was highly significant (p < 0.001). The first burst (heel stroke, hs) and the second burst (heel off, ho) did not show a significant difference for these conditions (Table 7). Although in three subjects there was also a 25% increase in vastus medialis (VM) of activity with head up, and a 20% decrease Table 1 Rectified and integrated EMG data were taken from all ten trials that the subjects performed and the peak amplitudes of the first. second and third burst for the different conditions averaged. Then the condihons were compared using a nonparametric statlstical test”. n.s. = not
sipnificant
Condition EMG (mV) Raseline Tonic Activit)
Significance
Head up
Head normal
p < 0.00 I
0.17+0.03
0.07~0.02
I.6fl.35
l.lto.30
Second burst (heel off)
n.5.
l).!)t0.25
l).7-tO.30
pio.01
2.0+0.45
I .5fO.25
p
X0%
32% I
these
findings
did
not
Head down condition. When the subjects walked with their heads pitched down, this third burst was not observed, and only minor EMG fluctuations were evident. With head turned to right or left, the variations from normal were even less significant. In conclusion, in all conditions except head up no variations of latencies and durations of the main activity bursts were found. Ground
reaction
force analysis
Normal vector diagram. During the stance phase of the normal stride, the evolution of vectors formed a typical, repetitive pattern (Figure 6, from left to right). Generally, it was made up by a monotonous advance of a point of application from the first vector, corresponding to heel contact (heel strike vector, HS), to the last one corresponding to toe off (HO). A characteristic feature of normal gait, despite the great complexity of the movement, was the smoothness of the profile of the vector’s progression. Two distinct maxima with a dip between them could be recognized, giving its envelope the typical ‘half-butterfly’ shape. During early stance the limb had to absorb the kinetic energy of the whole body by restraining the forward and downward motion of the centre of gravity. A force greater than the body weight Normal
n.s.
General probability of a third burst
gastrocnemius activity (GC), reach the level of significance.
675 ;
NW
a
_,__
:
If._iz: 0 ,__-%.3l
Head UP
Head down
walk!nq
713
First burst (heel stroke)
Third burst (middle of stance phase)
walking, with head down and with head up. a, Typical recording of all four and stride phases. The notations HS and HO signi+ heel strike and heel off.
NW
,,‘, /,, Ii, I i, “: I, _;
~___
:.,.,-KY o p’:,,f ,
757
_--_
NW
__
Figure 6 Comparison of force ground reactions in the conditions of normal walking, with head down and head up. a, Saggital vectograms; b, application points and linear regression
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lnjluence of otolith on gait: W.H. Zungemeister et al. Table 2 Median values (N) and significance of vector diagram differences. In principal, the same statiskal procedure was performed with the vector diagram results shown below as for Table 7. In Figure 6 each point of appli:ation is indicated either by a dot (lower half)& by the lower end of a vector (upper half). The linear progression proceeds from left to right. n.s. = not significant Condition Vector diagram
Significance
Head up
Head normal
First
pcro.001
710t61
550+5
Dip
n.s.
34Ok4.5
37Ok38
Second maximum
pco.03
753f50
715f32
1
and opposite to the direction of the movement was therefore needed (first maximum). In midstance, the centre of gravity underwent some sort of upward rebound, so that the ground reaction decreased with respect to body weight (dip). The subsequent push-off produced the last increase in ground-reaction amplitude, associated with a concentration of vectors on the metatarsi and with a forward inclination (second maximum). This behaviour showed slight interindividual differences. Head Up and Down Condilion. Data presented thus far have demonstrated that the ground reaction forces did not vary when the subjects walked with their heads normal, itched down or turned to the right or left. With hea B up all subjects produced a different shape of the saggital vectorgram characterized by a sharp transition from heel strike (first maximum) to toe off (second maximum), with significantly increased values (Table 2) of the first and second maximum. The first maximum was 710 compared to fi50N; for the second maximum it was 753 compared to 715 N; for the ‘dip’ there was no difference. In line with this finding is the concentration of vectors in the anterior part of the saggital vector-gram in relation to the appearance of the third activity burst of the tibialis anterior. In conjunction with this result, the application point progression was altered. All subjects showed a displacement of the application points toward the external of the foot during most of the stance phase, with a sharp transition at the end of the stance phase; statistically this observation was not significant. When the head was pitched down, subjects showed a saggital vectorgram whose shape demonstrated only minor similarities to the head-up condition described above. The transition seemed to be less marked but was still present. In this case there were no variations of the application point progression (Figure 6). The two subjects who also walked with eyes closed demonstrated a strong increase of activity of tibialis anterior and of the vastus medialis that was probably due to protective phenomena’“. There were no significant variations in the other muscle activities. The same behaviour as in the eyes-open condition was found for eyes closed with the head in the normal position and for eyes closed with head pitched up. The variations of ground reaction forces were the same as in the head up and eyes open condition.
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DISCUSSION Kinematic variables Kinematic changes were minor. The most significant result is the increase of the activity of the anterior muscles (TA and VM) with head-up. This effect could be caused by the backward displacement of the centre of gravity due to the new head position or it could be caused by vestibulospinal disinhibitionj excitation of the anti-gravity muscles/leg extensors because of a different net linear acceleration acting on range otoliths that were either out of their workin (Up), normal, or at their best working ‘iDown) position. The similarity of the results in the conditions of head up with eyes open or eyes closed (independently of the head position) made evident the role of vision during the walking cycle. In both situations an increase of anterior muscle activity and a displacement of the ground reaction forces towards the external foot is apparent. These phenomena could be due to a ‘research of equilibrium’ performed by the sub’ect trying to move forward the centre of gravity an d’ to increase the support area. With regard to the vectorgrams, the higher variations between maximum and minimum values can be explained by a higher acceleration of the centre of gravity. It is worthwhile to emphasize that such an increased acceleration of the centre of gravity does not correspond to a higher acceleration of the head. This demonstrates a lack of coordination. Other main characteristics of the vectorgram such as the concentration of vectors in the anterior part, may be correlated to the appearance of the third TA activity burst.
Previous experimental data about otolith influence on spinal-motoneuron excitability Change of position of the trunk with respect to the head and movement of the whole bodv in space evokes the tonic neck reflex and ves6bulospinal reflexes, respectively. It is well known that the pattern of reflex activity depends on the direction of the stimulus”“. For example, the tonic neck reflex evoked by pitch of the head of the decerebrate cat is believed to consist of bilateral forelimb extension and hindlimb flexion in the nose-up position, with the reverse for nose-down. In response to roll, the limbs towards which the chin points extend and the limbs towards which the vertex points flex. Consequently the question which arises is: how does the positian of the trunk versus the head, or the position of the whole body influence posture and gait? A feasible answer has been obtained as far as otolith reflexes are concerned. Polarization vectors, describing the direction of maximal tilt sensitivity, have been described for cat and monkey otolith afferents17”“. The directional selectivity and maximum sensitivity to head tilt of otolith afferent fibres and vestibular neurons including vestibulospinal neurons are well documented’7,‘“. The response of lumbar interneurons during tilting of the whole body has been investigated in the decerebrate catLO.The results show that the activity in lumbar interneurons is
In$uence ofotolith on gait: W.H.Zungemetiter et al. modulated during whole body tilt, and it was concluded that otolith receptors were the most probable candidates contributing to the observed responses. In this experiment gravity is the only force acting on the otolith end organs because the linear forward acceleration is close to zero with constant walking speed. Functionally, given the opposite effects of gravitational and tangential linear acceleration reaction forces on the otolith receptors, our results are in accordance with Nashner’s observations from translation perturbation studies. By preventing ankle joint movement during induced body sway using a twodegree-of-freedom, movable platform, Nashner examined how vestibular receptors contribute to postural stability. In the first 10Oms of body motion during a combination of forward platform translation and rotation, the body accelerates toe-u backwards’ P. It is probable that the effective force acting on the vestibular system during this period is largely a tangential linear acceleration, and in this situation the rapid backward sway stabilizing response causes a burst of activity in tibialis anterior and quadriceps. Soechting et al. ” showed in cats that contributions by the macular receptors to the motor output were the same when the orientation of the animal changed with respect to the gravitational field and when it was subjected to linear acceleration. This is the consequence of Newtonian mechanics. Under both conditions an increase in extensor activity occurs when the restoring shearing force is directed to the side ipsilateral to the limb, e.g. when the ipsilateal side is displaced upward during tilt about the longitudinal axis. Schema
of otolith neck counteraction
Following Roberts’ scheme” (Figure 7) otolith and neck influence would counteract. Only the relative contribution of each sensor would differ depending on the species and also on the particular condition, i.e. normal or pathological. Pathological cases might resemble neck influence, normal conditions might resemble otolith influence, as already demonstrated by Magnus”. Normally, with head up, legs and hip extend more, with head down, legs and hip extend less, or even flex (Figure 7, middle row). The similar rule with respect to neck reflex muscles would be valid for head rotation to left or right (the le contralateral to head rotation gets more ‘extended’ ‘i . Our results did not show this difference probably because neck influence in this maneuver is low and otolith input is the same for each condition. However, in patients with hemisyndromes, due, for example, to lesions of the internal capsule, this influence is high, as shown by Magnu8. This means that with dorsiflexion of the neck, legs are flexed, with ventriflexion on the neck, legs are extended. In the original Roberts scheme:< (upper left) there would be no influence as neck and otoliths counteract. This view of normal and abnormal conditions would re-enforce the results of Fuller’” and others, for four species stating that the neck-eye reflex is unreliable under normal conditions. It only becomes important with bilateral labyrinth loss. This fact has also been studied by Hansen and
Zangemeister’” with respect to a comparison of EEG activi that was related to body/neck movements with x ead immobile as compared to head/neck movements with body immobile. Almost no EEG response was obtained in the former case, but obvious head rotation evoked potentials were elicited with the latter manoeuvre. The athological condition refers to the work of Magnus Qsee ref. 2), who described the static neck reflexes in decerebrated cats and rabbits. Roberts” has developed his scheme using normal animals (cats, dogs) that were tilted on platforms or laid down in different positions. However he did not refer to experimental or clinical results in humans. In particular he did not note the fact of vestibular dominance over neck control in healthy humans. Clinical
considerations
A significant increase in excitability of lumbo-sacral motor nuclei due to spasticity assessed during quiet recumbency, might be lowered or eliminated during the execution of motor activities involving upright stance and walking’ with, in some instances, an unexpected functional outcome. Several observations support the concept that drug-induced amelioration of reflex hyperactivity does not necessarily result in improved dynamic function. A severely altered walking pattern far different from the normal might well be the best tactical solution in terms of functional daily ability’ ‘. Any restorative approach, either pharmacological or physiotherapeutical, should take this into account. Our results support the view that a functional linkage between otolith signals and activity in lower limb muscles is detectable during normal human gait. In healthy humans, otolith input appears to dominate other, particularly neck proprioceptive, influence this whereas in patients with CNS disturbances pattern may be reversed ‘. In human gait there are no more simple reflexes which characterize the behaviour of the decerebrate cat; probably during a voluntary movement there is a suppression of the vestibular and neck reflexes on the basis of past experiences and also of anticipation. In this way vestibular information is no longer directly influencing the motor set of the CNS during gait. As a consequence it was evident in our experiments that there is an increase of TA activity to increase safety. This offers more stability to counteract possible perturbations which under normal conditions are monitored and controlled through the vestibular s stem. The vector diagrams also demonstrated a ecrease of coordination during the movement dy caused by the larger displacement of the centre of gravity as demonstrated by the vector diagrams.
CONCLUSION The otolith input appears to particularly dominate neck proprioceptive and gaze motor influences during normal gait. This is demonstrated by an increase of tibialis anterior muscle activity during retroflexion of the head/neck, leading to an increase in stability and counteracting possible perturbations. It is also shown by a decrease of coordination during
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Influenceof otolithsongait: W.H. Zangemetiter et al.
the movement caused by larger displacement of the centre of gravity demonstrated in the vector diagrams. Postural control depends on the integration of vestibular, somatosensory and visual orientation signals. The otolith contribution to postural control is achieved by the integration of otolith inputs and peripheral afferent inputs involved in crossed reflex pathways. This study demonstrates that a functional linkage between otohth signals and activity in lower limb muscles is detectable in normal human gait.
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automatic movement tracking. In: Expert systems: Theory and applications Calgary: Acta Press, 1987: 225-7. Pedotti A. Simple equipment used in clinical practice for evaluation of locomotion. IEEE Trans Biomed Eng 1977; BME-24: 456-61. Boccardi S, Pedotti A, Rodano R, Santambrogio GC. Evaluation of muscular moments at the lower limb joints by an online processing of kinematic data and ground reactions. JBiomech 1981; 14: 35-45. Pedotti A. A study of motor coordination and neuromuscular activities in human locomotion. Biol Cybern 1977; 26: 53-62. Weber E. Grundriss der biologischen Statistik. Stuttgart: Fischer, 1967: 269-77. Conrad B, Benecke R, Meinck HM, Cranehl E, Hohne J. Problematik Quantifizierung zentraler Zur der uberschuss-Syndrome. In: Struppler A, ed. Elektrophysiologische Diagnostik in der Neurologie New York: Thieme, 1!182: 206-!I. Fernandez C, Goldberg J. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. J Neurophysiol 1976; 39: 985-9.5. Tomko D, Peterka R, Schor R. Responses to head tilt in cat eighth nerve afferents. Exp Brain Res 198 1; 41: 2 1(i-2 1. Schor R, Miller A. Vestibular reflexes in neck and forelimb muscles evoked by roll tilt. J Neurophysiol l!Nl; 46: 167-78. Suzuki J, Timerick SJB, Wilson VJ. Body position with respect to the head or body position in space is coded by lumbar interneurons. J Neurophysiol 1!)85; 54: 123-33. Nashner L, Forssberg H. Phase-dependent organization of postural adjustments associated with arm movements while walking. J Neurophysiol l!IX6; 55: 138%!14. Soechting JF, Anderson JH, Berthoz A. Dynamic relations between natural vestibular inputs and activity of forelimb extensor muscles in the decerebrate cat. Motor output during rotation in the vertical plane. Brain Res 1!)77; 120: 35-47. Fuller J, Maldonado H, Schlag J. Vestibular-oculomotor interaction in cat eye-head movements. Exp Brain Res l!j83; 271: 241~ii0. Hansen HC, Zangemeister WH, Kunze K. Cortical activity in response to voluntary stimulation of vestibular, cervical and brachial proprioceptors In: Kunze, K, Zangemeister WH, Arlt A, eds. Clinical Problems of Brain-stern Disorders New York: Thieme, 1!)86: 213-18.
I!)9
I, accepted
M.V. Bulgheroni’.
influenced
and A. Pedotti’
Clinic, Hamburg, Germany; .‘Centro di Don C. Gnocchi e Politecnico di Milano, Italy May
by the
Bioengegneria,
I Ii!)1
ABSTRACT Postural control depends on the integration of vestibular, somatosensory and visual orientation signals. The otolith contribution topostural control is achieved by the integration of otolith inputs andperipheral afferent inputs involved in crossed reJex pathways. This study shows that a functional linkage between otolith signals and activity in lower limb muscles is detectable in normal human gait. The otolith input appears to dominate particularly the neck proprioceptive and gaze motor influences during normal gait. This is demonstrated by an increase of tibialis anterior muscle activi[y during retrojlexion of the head/neck, leading to an increased stability and counteracting possible perturbations. It is also shown by decrease of roordination during the movement caused b.v larger displacement of the centre of gravity demonstrated in vector dia
Gait analysis,
vestibular-neck-influence
on gait. kinematical-EMG-forceplate
INTRODUCTION When a human being experiences a change of posture, the vestibular system can only initiate appropriate body postural reflexes if the relative position between the labyrinths and the body is known. A continuous flow of information from neck proprioceptors and other position receptors of the vertebral column is thus essential for a proper functioning of the vestibular system. Such afferents interact with postural control circuits of the brain stem at various levels, including the vestibular nuclei, thereby not only gaining access to neuronal substrates which guide postural reflexes of the body but also to circuits mediating such reflexes of the oculomotor and gaze motor system. The vestibular system monitors the forces associated with angular and linear acceleration of the head by means of five organs located within the labyrinthine cavities of the temporal bones on each side of the skull. The saccular and urticular sense linear acceleration, and the cristae of the three semicircular canals sense angular acceleration of the head. The capacity of the maculae and cristae to function as sensors of linear and angular acceleration, respecconfiguration’. tively, rests on their anatomical When we reviewed the literature with respect to the influence of vertical head/eye posture on gait, most data referred to the otoliths’ influence on postural activities during stance. Clear information on their influence on gait, especially in humans, is lacking and in this study two questions were pursued. Correspondence and reprint requests to: Prof. Dr W.H. Zangemeister, Neurological University Clinic Hamburg-Eppendorf, Martinistr. 52, D 2000 Hamburg 20, Germany @ I!)!)1 Butterworth-Heinemann ol~l-s12T,/!~l/olio~lil-ox
analysis,
gaze-gait
control
When normal humans walk under three different conditions of vertical head posture, i.e. primary position, 45” anteflexion, 45” retroflexion, would it be ossible to distinguish for these subjects responses besides the general arousal effect of this manoeuvre) P that resemble clinical intuitive observations from patients with different kinds of spasticity as reported in the early literature”.” (Figure 7). Secondly, how could such results fit into recent observations on the linkage between gaze position, otolith influences and neck muscles as the upper most part of the truncal/ skeletal muscles”‘?
METHODS In order to develop a precise analysis of human gait under different conditions we used the ELITE system, a motion analyser (Figure 2). This system allows a multifactorial analysis of the walking cycle by means of simultaneous acquisition and processing of TV images and analogue signals from a force platform and an EMG unit. The core of the system is an image processor which analyses the frames coming from two TV cameras’“. It detects the presence and the position of passive markers worn by the subject in real time. The special algorithm of bi-dimensional crosscorrelation adopted in the ELITE system to detect the position of markers allows one to obtain a very high precision and accuracy. To quantify this accuracy, special tests were performed. They consisted of measuring the distance between spherical markers fixed to a rigid body in static and dynamic conditions. In the operative conditions two TV cameras were
for BES J. Biomed.
Eng. 1991. Vol. IS. November
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Injluence of otolith
on gait: W.H. Zangemeister et al Labyrmth
Neck Head up
Dowflexed
Head down
Head narmal
T-f
b
a Normal
d
’
e
Ventnflexed
h
g
C
I
I
f
\
P-
Figure 1 Schema of combined effects on limbs produced by the positional reflexes from the neck and from the labyrinth (right lateral views) (both modified from ref. 3). Note that the row labelled neck normal, d, e, f, represents the normal otolith dominance with legs flexed/head up and legs extended/head down. The column headed head normal, b, e, h, represents the pathological condition of neck static dominance. This refers to Magnus’ and his results regarding neck reflexes in decerebrated mammals. Our experimental condition for bipedal gait with respect to the antigravity muscles would be depicted in d and f. The neck normal condition obviously has been sketched by Roberts’ in a simplified way for easy understanding of the concept. Of course, in most quadrupedal mammals the neck normal condition would refer to a head retroflexion of about Ii;“. In humans the neck normal condition applies to an approximately 15” anteflexion of the head
used (SD acquisition) and we obtained the following results. In the static condition (motionless object in different parts of the field of view) the average measurement precision of the marker position is one part on 19 750 and in the dynamic condition (object moving through the field of view) the average measurement precision of marker position is one part on 2800. During these experimental trials the two TV
cameras were placed at a distance of about 5m on one side of the walking pathway. They were 5 m away from each other and were placed at a height of about 1 m from the ground. Fifty frames per second were processed in real time by the ELITE system for each TV camera. The coordinates of the detected markers were sent to the host computer, a Digital PDPl l/73, where a second level processing took place. A complex tracking procedure allowed a completely automatic classification of the markers and the reconstruction of their trajectories even when some markers were temporarily hidden or their trajectories intersected’ ‘. After the classification of the markers recognized by each TV camera, the system performed the three dimensional reconstruction and the computing of linear velocities and accelerations for each marker and each frame. The ground reaction forces (GRF) were recorded by means of a Kistler force platform. The signals from the transducers were sent to a charge amplifier connected to the host computer. The sampling frequency of the data from the charge amplifier was FiOHz. The host computer processed the acquired data to compute the components of the ground reaction forces Fx, Fy and Fz and the progression of their application point on the platform surface. These results were globally represented as two vectograms which illustrate the space evolution of the ground reaction forces in the sagittal and in the frontal planel4 13. The myoelectric signals were recorded by means of a telemetric system composed by an EMG receiver and by a portable unit worn by the sub’ect that was directly connected to the surface electro d es placed on the muscular masses of interest. The bandpass of the EMG system used was 16-2.50Hz. The signals from the receiver were sampled by the host computer with
EMG receiver
Kinematical
TV
reports
camera TV camera 2 Force platform
1
processor
,
L] Dynamical
reports
Charge amplifier
EMG reports Figure 2 An overview of the ELITE system. The subject moves in the field of view of two TV cameras to allow a three dimensional analysis of his motion. He wears retroflective markers on the anatomical points of interest. The image processor recognizes these markers and sends their coordinates to the host computer for further elaborations. The subject also wears surface electrodes connected to a portable EMG transmitter. The myoelectric signals are filtered and amplified by the receiver and then sent to a computer. The signals coming from the force platform are preprocessed by the charge amplifier. The components of the ground reaction forces and their application points are then sent to the computer. After a second level processing, different reports of the measured data are ready for output
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Injkmce of otolith on guit: W.H. Zungemeisteret al.
a frequency of ,500 H z. The resolution of the A/D converter was 12 bits for all the 16 analogue signals (8 channels for ground reactions and 8 channels for myoelectric activities). During the experimental trials the subject wore 10 markers placed on cheek bone, jaw corner, shoulder, elbow, hip, trocanter, knee, ankle, heel and fifth metatarsal head of the right leg. The surface electrodes were placed on the vastus medialis (VM), biceps femoris (BF), tibialis anterior (TA) and gastrocnemius (GC) of the same leg. To prevent artifacts and electrical noise the electrodes were placed after cleaning, depilation and scraping of the skin. An analogue integrator provided the rectified and integated EMG signals while a simple resistances’ circuit placed under the shoe sole made it possible to reconstruct the phases of walking cycle that were also recorded on an X-channel UV recorder.
cadence. For each condition the subject performed at least IO trials. For comparison with quiet stance conditions, the subject was asked to stand for few seconds (30-60s) in each of the conditions described above while EMG and VDT were performed. Quantification of head posture was done by using the ELITE system. We examined five subjects who were 27 & 8 years old. They were all right-handed and, to guarantee homogeneous starting conditions, wore tennis shoes. For the analysis of the data we considered kinematic, dynamic and myoelectrical parameters. As far as kinematics are concerned we analysed trajectories, velocities and accelerations of all markers worn by the subject, particularly in the forward direction. Concerning dynamics we chose to focus on the progression of the application point and on the trend of the force path. The analysis of the myoelectrical activity was executed on the raw signal and on the rectified and integrated signal. By analogue instrumentation the signal was filtered in the range of ‘LO-250 Hz with an amplifier gain of 2500. Integration was obtained by analogue means as well with a time constant of .50 ms. After preprocessing the data in that fashion, we focused attention on the main myoelectric parameters such as amplitude, duration and latency of the most significant activity bursts.
Test procedure At the beginning the subject was asked to walk at a natural cadence for some steps in order to obtain ten recordings of gait in normal conditions, demonstrating the repeatability of gait parameters under normal conditions. The condition for the second set of trials was with head placed 45” down. In the third condition the subject walked with head placed 4.5” up. The last two sets of walking cycles were performed with the head turned X0” towards the right and left, respectively. In all these conditions there were no variations in gaze direction, i.e. the eyes were looking straight ahead, and walking
Normoi
RESULTS The kinematic analysis was based on the examination velocities and accelerations of all of trajectories, markers. Comparison between the quantitative kine-
Head down
wolkq
I
I
Heod up
7
Figure 3 Comparison of kinematic parameters in the conditions of normal walking, with head down and with head up. a, stick diagrams; b, X coordinates of leg markers; the measured length stride is reported in millimetres. (H, heel; M, lateral malleolus; Vm, F’th metatarsal head; K, knee; T, trochanter; Hi, hip, iliac crest. These last two markers are practically always superimposed. The same terminology applies to the subsequent three figures. c, Y coordinates of leg markers. The coordinates of the markers are measured in mm. The upper marker corresponds to the iliac crest, the second to the trochanter, the third to the knee, the fourth to the malleolus, the fifth to the Vth metatarsal head and the last to the heel
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Injluence of otoliths on gait:
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matic data obtained for every single condition ensured a high repeatability of their trend. Figure 3 shows a stick diagram and trajectories of leg markers during three trials performed in normal conditions, with head down and with head up, respectively. The stick diagram clearly shows the different head posture in these three conditions. In the first column, where the condition of normal walking is depicted, it is possible to compute a reference value of inclination which defines the normal vertical position. This value is obtained by computing the angle between the segment linking the two head markers and the vertical direction. In the other rows of Figure 3 the X and Y coordinates of the leg markers in the three main conditions are compared. The X axis is coincident with the walking direction, while the Y axis is the vertical axis. In Figure 3b the trajectories of leg markers along the walking direction are depicted. The difference between the motion of the upper (hip and greater trochanter) markers and the motion of the lower ones (knee and foot markers) is evident. Upper markers show a linear trend (uniform velocity) while knee and foot markers show some oscillations around a straight line. With regard to the foot trajectories, it is easy to distinguish the stance phase, i.e. when the values for the X coordinates do not vary and the swing phase, when the same values increase almost linearly. In Figure 3c, the upper markers demonstrate a slight periodic vertical oscillation and a similar path, while the foot markers show larger height variations during the swing phase. The 2 coordinates are not illustrated because walking develops mainly on a straight line and displacements in the horizontal plane are not significant. There are practically no variations for all the coordinates. The same is also true for velocities and accelerations (Figure 4). In Figure 4a the velocities along the walking direcof the upper markers tion’ are shown. The velocit (hip and greater trochanter r is almost constant as suggested by the linear trajectories, while the foot markers show a velocity peak in the middle of the swing phase. Obviously their velocity becomes zero during stance phase. In the vertical direction (Figure 4b) the only significant variations of velocity are during the swing phase and even in this direction, the most typical behaviour is shown by the foot markers displaying three velocity peaks: two of them have positive values and take place at the beginning and at the end of the swing phase, while a negative one characterizes the middle of the swing phase. (Fi ure 4c,d), a With regard to head accelerations periodic trend in these directions (.Kand ys is evident. It was observed that the amplitude of the acceleration in the x direction was low for head up compared to head down, and increased in the y direction, respectively, for head up. In Figure 4c,d, the extrema and zero-crossings of x and y head accelerations appear to be about 180” out of phase. This was true for all conditions with only slight variations between down and up. Because the utricule is close to its optimum working range in the down position and, conversely, out of its working range in the up position a different compound linear acceleration vector would result, if the effect of
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L
a
b
Comparisonof kinematical parameters in the conditions of normal walking, with head down and with head up. a, Velocities in the X direction of leg markers; b, velocities in the Y direction of leg markers; c, acceleration in X direction of the upper head (cheekbone) marker; d, acceleration in the Y direction of the upper head (cheekbone) marker. The velocities of the markers are measured in mms ’ and the accelerations in mms ‘. Values of velocity and acceleration are represented by using a self-adjusting technique, so that each diaFam is scaled to its range of variation Figure 4
gravity is taken into account given similar acceleration dynamics for all conditions. Thus different otolith stimulations should result in a change of leg EMG activities. However, there were no variations even in stride length. The same results were obtained for head turning to the right and to the left. All respective results were reproducible in all subjects.
EMG analysis The analysis of the myoelectric recordings demonstrated distinct differences particularly in the head up condition (Figure 5). Normal condition. The comparison with torques at joints clarified the information content of the EMG, especially regarding the intersubject features and the sequence of muscle activation. Even with qualitative analysis of the EMG signals it appeared that, despite similar kinematics and speed, the EMG patterns of different subjects were in agreement with the respective torques computed by the mathematical model. This was in line with the results reported by Pedotti’ ‘. The main neuromuscular events beyond the normal expected statistical variation could be thus established in a precise way. Inaccuracies due to the recording procedure could also be reasonably excluded. Head up condition. With the head up all sub‘ects showed a significant increase of tibialis anterior iTA)
Figure 5 Comparison of EMG activittes in the conditions muscles and stride phases; b, typical rectified and integrated respectively
of normal recordings
activity (Table 7). In addition to a significant I b < w3.l 1) general increase of tonic activity of TA &ring the whole walking cycle, the most interesting phenomenon was the appearance of a third activity burst in the middle of the stance phase. The amplitude of such a burst ranged from 1.1 to 2..5 mV and its duration from 90 to 320ms. This phenomenon was, in general, present in the recordings of all subjects. This was not seen under other conditions. A nonparametric statistical analysis (Table 7, Wilcoxon test’“) on the probability of the appearance of such a third burst demonstrated that under normal conditions it occurred in 32% of cases. However, in the head up condition, it occurred in 80% of cases, with head down in 23%) of cases. This difference was highly significant (p < 0.001). The first burst (heel stroke, hs) and the second burst (heel off, ho) did not show a significant difference for these conditions (Table 7). Although in three subjects there was also a 25% increase in vastus medialis (VM) of activity with head up, and a 20% decrease Table 1 Rectified and integrated EMG data were taken from all ten trials that the subjects performed and the peak amplitudes of the first. second and third burst for the different conditions averaged. Then the condihons were compared using a nonparametric statlstical test”. n.s. = not
sipnificant
Condition EMG (mV) Raseline Tonic Activit)
Significance
Head up
Head normal
p < 0.00 I
0.17+0.03
0.07~0.02
I.6fl.35
l.lto.30
Second burst (heel off)
n.5.
l).!)t0.25
l).7-tO.30
pio.01
2.0+0.45
I .5fO.25
p
X0%
32% I
these
findings
did
not
Head down condition. When the subjects walked with their heads pitched down, this third burst was not observed, and only minor EMG fluctuations were evident. With head turned to right or left, the variations from normal were even less significant. In conclusion, in all conditions except head up no variations of latencies and durations of the main activity bursts were found. Ground
reaction
force analysis
Normal vector diagram. During the stance phase of the normal stride, the evolution of vectors formed a typical, repetitive pattern (Figure 6, from left to right). Generally, it was made up by a monotonous advance of a point of application from the first vector, corresponding to heel contact (heel strike vector, HS), to the last one corresponding to toe off (HO). A characteristic feature of normal gait, despite the great complexity of the movement, was the smoothness of the profile of the vector’s progression. Two distinct maxima with a dip between them could be recognized, giving its envelope the typical ‘half-butterfly’ shape. During early stance the limb had to absorb the kinetic energy of the whole body by restraining the forward and downward motion of the centre of gravity. A force greater than the body weight Normal
n.s.
General probability of a third burst
gastrocnemius activity (GC), reach the level of significance.
675 ;
NW
a
_,__
:
If._iz: 0 ,__-%.3l
Head UP
Head down
walk!nq
713
First burst (heel stroke)
Third burst (middle of stance phase)
walking, with head down and with head up. a, Typical recording of all four and stride phases. The notations HS and HO signi+ heel strike and heel off.
NW
,,‘, /,, Ii, I i, “: I, _;
~___
:.,.,-KY o p’:,,f ,
757
_--_
NW
__
Figure 6 Comparison of force ground reactions in the conditions of normal walking, with head down and head up. a, Saggital vectograms; b, application points and linear regression
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lnjluence of otolith on gait: W.H. Zungemeister et al. Table 2 Median values (N) and significance of vector diagram differences. In principal, the same statiskal procedure was performed with the vector diagram results shown below as for Table 7. In Figure 6 each point of appli:ation is indicated either by a dot (lower half)& by the lower end of a vector (upper half). The linear progression proceeds from left to right. n.s. = not significant Condition Vector diagram
Significance
Head up
Head normal
First
pcro.001
710t61
550+5
Dip
n.s.
34Ok4.5
37Ok38
Second maximum
pco.03
753f50
715f32
1
and opposite to the direction of the movement was therefore needed (first maximum). In midstance, the centre of gravity underwent some sort of upward rebound, so that the ground reaction decreased with respect to body weight (dip). The subsequent push-off produced the last increase in ground-reaction amplitude, associated with a concentration of vectors on the metatarsi and with a forward inclination (second maximum). This behaviour showed slight interindividual differences. Head Up and Down Condilion. Data presented thus far have demonstrated that the ground reaction forces did not vary when the subjects walked with their heads normal, itched down or turned to the right or left. With hea B up all subjects produced a different shape of the saggital vectorgram characterized by a sharp transition from heel strike (first maximum) to toe off (second maximum), with significantly increased values (Table 2) of the first and second maximum. The first maximum was 710 compared to fi50N; for the second maximum it was 753 compared to 715 N; for the ‘dip’ there was no difference. In line with this finding is the concentration of vectors in the anterior part of the saggital vector-gram in relation to the appearance of the third activity burst of the tibialis anterior. In conjunction with this result, the application point progression was altered. All subjects showed a displacement of the application points toward the external of the foot during most of the stance phase, with a sharp transition at the end of the stance phase; statistically this observation was not significant. When the head was pitched down, subjects showed a saggital vectorgram whose shape demonstrated only minor similarities to the head-up condition described above. The transition seemed to be less marked but was still present. In this case there were no variations of the application point progression (Figure 6). The two subjects who also walked with eyes closed demonstrated a strong increase of activity of tibialis anterior and of the vastus medialis that was probably due to protective phenomena’“. There were no significant variations in the other muscle activities. The same behaviour as in the eyes-open condition was found for eyes closed with the head in the normal position and for eyes closed with head pitched up. The variations of ground reaction forces were the same as in the head up and eyes open condition.
456’ J. Biomed. Eng. 1991, Vol. 13. November
DISCUSSION Kinematic variables Kinematic changes were minor. The most significant result is the increase of the activity of the anterior muscles (TA and VM) with head-up. This effect could be caused by the backward displacement of the centre of gravity due to the new head position or it could be caused by vestibulospinal disinhibitionj excitation of the anti-gravity muscles/leg extensors because of a different net linear acceleration acting on range otoliths that were either out of their workin (Up), normal, or at their best working ‘iDown) position. The similarity of the results in the conditions of head up with eyes open or eyes closed (independently of the head position) made evident the role of vision during the walking cycle. In both situations an increase of anterior muscle activity and a displacement of the ground reaction forces towards the external foot is apparent. These phenomena could be due to a ‘research of equilibrium’ performed by the sub’ect trying to move forward the centre of gravity an d’ to increase the support area. With regard to the vectorgrams, the higher variations between maximum and minimum values can be explained by a higher acceleration of the centre of gravity. It is worthwhile to emphasize that such an increased acceleration of the centre of gravity does not correspond to a higher acceleration of the head. This demonstrates a lack of coordination. Other main characteristics of the vectorgram such as the concentration of vectors in the anterior part, may be correlated to the appearance of the third TA activity burst.
Previous experimental data about otolith influence on spinal-motoneuron excitability Change of position of the trunk with respect to the head and movement of the whole bodv in space evokes the tonic neck reflex and ves6bulospinal reflexes, respectively. It is well known that the pattern of reflex activity depends on the direction of the stimulus”“. For example, the tonic neck reflex evoked by pitch of the head of the decerebrate cat is believed to consist of bilateral forelimb extension and hindlimb flexion in the nose-up position, with the reverse for nose-down. In response to roll, the limbs towards which the chin points extend and the limbs towards which the vertex points flex. Consequently the question which arises is: how does the positian of the trunk versus the head, or the position of the whole body influence posture and gait? A feasible answer has been obtained as far as otolith reflexes are concerned. Polarization vectors, describing the direction of maximal tilt sensitivity, have been described for cat and monkey otolith afferents17”“. The directional selectivity and maximum sensitivity to head tilt of otolith afferent fibres and vestibular neurons including vestibulospinal neurons are well documented’7,‘“. The response of lumbar interneurons during tilting of the whole body has been investigated in the decerebrate catLO.The results show that the activity in lumbar interneurons is
In$uence ofotolith on gait: W.H.Zungemetiter et al. modulated during whole body tilt, and it was concluded that otolith receptors were the most probable candidates contributing to the observed responses. In this experiment gravity is the only force acting on the otolith end organs because the linear forward acceleration is close to zero with constant walking speed. Functionally, given the opposite effects of gravitational and tangential linear acceleration reaction forces on the otolith receptors, our results are in accordance with Nashner’s observations from translation perturbation studies. By preventing ankle joint movement during induced body sway using a twodegree-of-freedom, movable platform, Nashner examined how vestibular receptors contribute to postural stability. In the first 10Oms of body motion during a combination of forward platform translation and rotation, the body accelerates toe-u backwards’ P. It is probable that the effective force acting on the vestibular system during this period is largely a tangential linear acceleration, and in this situation the rapid backward sway stabilizing response causes a burst of activity in tibialis anterior and quadriceps. Soechting et al. ” showed in cats that contributions by the macular receptors to the motor output were the same when the orientation of the animal changed with respect to the gravitational field and when it was subjected to linear acceleration. This is the consequence of Newtonian mechanics. Under both conditions an increase in extensor activity occurs when the restoring shearing force is directed to the side ipsilateral to the limb, e.g. when the ipsilateal side is displaced upward during tilt about the longitudinal axis. Schema
of otolith neck counteraction
Following Roberts’ scheme” (Figure 7) otolith and neck influence would counteract. Only the relative contribution of each sensor would differ depending on the species and also on the particular condition, i.e. normal or pathological. Pathological cases might resemble neck influence, normal conditions might resemble otolith influence, as already demonstrated by Magnus”. Normally, with head up, legs and hip extend more, with head down, legs and hip extend less, or even flex (Figure 7, middle row). The similar rule with respect to neck reflex muscles would be valid for head rotation to left or right (the le contralateral to head rotation gets more ‘extended’ ‘i . Our results did not show this difference probably because neck influence in this maneuver is low and otolith input is the same for each condition. However, in patients with hemisyndromes, due, for example, to lesions of the internal capsule, this influence is high, as shown by Magnu8. This means that with dorsiflexion of the neck, legs are flexed, with ventriflexion on the neck, legs are extended. In the original Roberts scheme:< (upper left) there would be no influence as neck and otoliths counteract. This view of normal and abnormal conditions would re-enforce the results of Fuller’” and others, for four species stating that the neck-eye reflex is unreliable under normal conditions. It only becomes important with bilateral labyrinth loss. This fact has also been studied by Hansen and
Zangemeister’” with respect to a comparison of EEG activi that was related to body/neck movements with x ead immobile as compared to head/neck movements with body immobile. Almost no EEG response was obtained in the former case, but obvious head rotation evoked potentials were elicited with the latter manoeuvre. The athological condition refers to the work of Magnus Qsee ref. 2), who described the static neck reflexes in decerebrated cats and rabbits. Roberts” has developed his scheme using normal animals (cats, dogs) that were tilted on platforms or laid down in different positions. However he did not refer to experimental or clinical results in humans. In particular he did not note the fact of vestibular dominance over neck control in healthy humans. Clinical
considerations
A significant increase in excitability of lumbo-sacral motor nuclei due to spasticity assessed during quiet recumbency, might be lowered or eliminated during the execution of motor activities involving upright stance and walking’ with, in some instances, an unexpected functional outcome. Several observations support the concept that drug-induced amelioration of reflex hyperactivity does not necessarily result in improved dynamic function. A severely altered walking pattern far different from the normal might well be the best tactical solution in terms of functional daily ability’ ‘. Any restorative approach, either pharmacological or physiotherapeutical, should take this into account. Our results support the view that a functional linkage between otolith signals and activity in lower limb muscles is detectable during normal human gait. In healthy humans, otolith input appears to dominate other, particularly neck proprioceptive, influence this whereas in patients with CNS disturbances pattern may be reversed ‘. In human gait there are no more simple reflexes which characterize the behaviour of the decerebrate cat; probably during a voluntary movement there is a suppression of the vestibular and neck reflexes on the basis of past experiences and also of anticipation. In this way vestibular information is no longer directly influencing the motor set of the CNS during gait. As a consequence it was evident in our experiments that there is an increase of TA activity to increase safety. This offers more stability to counteract possible perturbations which under normal conditions are monitored and controlled through the vestibular s stem. The vector diagrams also demonstrated a ecrease of coordination during the movement dy caused by the larger displacement of the centre of gravity as demonstrated by the vector diagrams.
CONCLUSION The otolith input appears to particularly dominate neck proprioceptive and gaze motor influences during normal gait. This is demonstrated by an increase of tibialis anterior muscle activity during retroflexion of the head/neck, leading to an increase in stability and counteracting possible perturbations. It is also shown by a decrease of coordination during
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Influenceof otolithsongait: W.H. Zangemetiter et al.
the movement caused by larger displacement of the centre of gravity demonstrated in the vector diagrams. Postural control depends on the integration of vestibular, somatosensory and visual orientation signals. The otolith contribution to postural control is achieved by the integration of otolith inputs and peripheral afferent inputs involved in crossed reflex pathways. This study demonstrates that a functional linkage between otohth signals and activity in lower limb muscles is detectable in normal human gait.
12.
13
14
15. 16
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