REVIEWS
PHYSIOLOGICAL
Vol.
55, No. 2, April 1975 Printed in U.S. A.
Locomotion Mechanisms
Central
in Vertebrates: and Reflex Interaction
S. GRILLNER Department I. II.
IV. V.
VI.
VII.
IX. X.
I.
of Giiteborg,
Gb’teborg,
Sweden 247 248 248
Electromyography...............................................
C. Forces. ........................................................ Movements of Entire Animal : Interlimb Coordination. A. In-phase gaits. .................................................. B. Comparative aspects of locomotion. ................................ C. How is interlimb coordination achieved in D. Bipedal locomotion. ............................................. Locomotion in Decorticate and Mesencephalic A. Locomotion Deafferentation mechanisms
in acute high experiments .........
...................
Preparations
259 260 262
C. D. E.
Mammals. ..................................................... Fishes. ......................................................... Comments and conclusions. ......................................
265 266 267
..............
decerebrate cats. ......................... and other evidence for central ........................................
Amphibians. Reptiles
and
251 253 256
tetrapods? ..................
A. B.
locomotor 272 272
.................................................... birds. ..............................................
273 274 275 276 277 277 279
Locomotor Capacity of Spinal Cord. .................................. A Fishes and lower chordates. ....................................... B. Amphibians ..................................................... C. Reptiles and birds. .............................................. D. Mammals Central Pattern A. B.
VIII.
University
Introduction ....................................................... Step Cycle of the Individual Limb. ................................... ~2. Kinematics. .................................................... B.
I I I.
of Physiology,
Brown’s Neuronal
...................................................... Generator for Locomotion
.............................
Significance .A. Peripheral B. Systems C. Possible
and its development. ............................ possibly related to generation of locomotion. ......... ........................ of Peripheral Input in Locomotion. inputs influencing step cycle and gait. .................... taking part in autoregulation of muscle activity. .............. phasic control of reflex arcs related to step-cycle reflex reversals.
D. Reflexes Descending A. Descending
that have been related to locomotion: negative findings. ....... Control of Spinal Locomotion Circuitry. ..................... systems possibly responsible for tonic activation. ...........
Concluding
279 280 282 284 285
hypothesis activity
Remarks
...............................................
287 288 290 ..
290 291 293 294 295
INTRODUCTION
During ambulation an animal has to deal with at least three different tasks. I) It must perform the actual locomotor movements of the different limbs according to a rather stereotyped plan. 2) It must adapt these movements to external condi247
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248
S. GRILLNER
Volume
55
tions in order to accomplish purposeful locomotion so as to achieve various goals such as catching prey or escaping an enemy. Furthermore in almost each step cycle adjustments must be made to place the limb properly, e.g., on a stone and not in a hole; i.e., the animal must continously anticipate where to put down the foot. 3) It must maintain equilibrium during the movements; i.e., the projection of the center of gravity must fall in an optimally stable point between the moving points of support and be maintained within rather narrow limits. In order to accomplish this a whole set of different compensating mechanisms has evolved that enables the animal to counteract various types of unexpected perturbations. This review deals almost exclusively with the first task-i.e., how does the central nervous system generate the actual locomotor movements. I have attempted to compare the different classes of vertebrates in order to extract the common features that emerge. It is natural that some pertinent work might have been excluded, since it is possible only to cover some general aspects and approaches, i.e., those that the reviewer at present has felt as the most important. Flight in vertebrates has not been considered but the reader is referred to the interesting review of Pennycuick (197) for the mechanical aspects of flight. In order to have any reasonable chance to understand the underlying nervous mechanisms, we must first know what movements are actually perf’ormed by the individual limbs and how the limbs are coordinated. Which factors change at different speeds and which factors remain constant? What are the time constraints, the forces, and the contribution of individual muscles? Therefore this type of basic information is considered first in order to be able to later consider central mechanisms.
II.
STEP
CYCLE
OF
THE
INDIVIDUAL
LIMB
A. Kinematics The limbs serve two purposes during locomotion: to support the body during the ongoing movement as the wheels of a carriage and to generate the propulsive force for progession to take place. The actual locomotor movements were analyzed cinematographically by Philippson (205), who measured how the different jcint angles change with time (see Fig. 1). Just after the foot leaves the ground a flexion occurring in knee, ankle, and hip brings the limb forward to a more rostra1 postion [i.e., the flexion phase (F)], where the knee and ankle start to extend and somewhat later the hip [i.e., the start of the extension phase (E)]. This phase is divided into three parts: Er, during which the limb is extended and brought down to contact with ground; Ez, when the knee and ankle flex somewhat, yielding under the weight of the body after contact; E 3, during which the limb extends again and This classification scheme has been used by many pushes the animal forward. subsequent authors (66, 67, 83, 160), but other terms are frequently used (see Fig. 1). It should be noted that the foot is in contact with the ground only in EZ and Es (stance or support phase) and is off the ground in F and Er (swing or
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April
1975
CONTROL
OF
249
LOCOMOTION
transfer phase). Flexion and protraction are often used as synonyms as well as retraction and extension (Fig. 1). Some authors utilize this terminology when describing particularly the hip movement, which differs from that of the knee. The E2 phase appears to be purely passive since during stepping movements in the air only one single extension movement occurs (205). Thus when the limb does not have to carry the weight under which it yields, no ET is found. The same is true during movement in another homogeneous medium such as swimming in water (172). The cat always uses the forefoot as support (digitigrade), whereas other animals such as the bear or humans put down their heels first in walking (plantigrade support). It is interesting that during running there is a shift to digitigrade locomotion. The leg movements are similar in principle (28, 16 1, 162) in both cases and the Philippson step cycle has been applied to humans (119). The limb movements for amphibians and reptiles, though not as well studied, are considered further below (interlimb coordination). They differ fundamentally in that the femur and humerus point laterally and the movement of the limb is similar to that of a spoke of a horizontal wheel being brought back and forth (90). Arshavsky et al. (11) studied the step cycle of fore- and hindlimbs in order to quantify the step-cycle changes with the speed of locomotion and to determine if certain parts of the cycle would be constant and others speed dependent (dogs). The animals walked on a treadmill that could be set at different constant velocities. walk
0.6 m/s
gallop
0I
150 130 -
XX
XX
X
7.3 m/s
150 130
0 ;
II0
I
0
I IO
.x
Lo,
I k E
.-
90
.-0
70
11 :F:E, I 8 :flexion: + : pro- :+--, I :4- swing ++: +-transfer++
FIG.
slow
walk
90
0
X’ x
;y2: ’ extension retraction
hatched region. walk and gallop, of step cycle are
limb is drawn for account movement
x hip l ankle
70
I I I
stance
,
support
1. Step cycle. Joint angles and a fast gallop [replotted
is indicated by phase) between different phases
E3
I
in ankle and from Goslow
hip are plotted throughout et al. (83)]. Below graphs
one period
Note striking difference in duration of contact whereas swing phase remains constant. Different listed below graph. Under right graph approximate
the different phases indicated of lower spine (see text).
by interrupted
lines.
Drawings
step cycle in a of foot contact period terms do not
(stance used for position of take
into
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250
S. GKILLNEK
Volume
55
B 200
L F
IO0
El
0
2
4
velocity FIG.
swing which
0
in step
at different marked
24
velocity
(m/s)
2. Changes
and stance is particularly
6
cycle
with
0
6
(m/s)
different
2
4
velocity forward
velocities
forward velocities. Note marked for ES (shown in C). Swing phase
6
0
I234 velocity
(m/s) of locomotion.
(rds)
A; duration
of
speed dependence of stance phase, is virtually constant; although El
varies somewhat, F is constant (shown in H). D: step length is plotted (i.e., total step-cycle tion X velocity) at different speeds and below is distance traveled during each stance phase duration of stance X velocity). A-C are from the cat [replotted from Goslow et al. phase D is from the dog [from Arshavsky et al. (1 l)].
dura(i.e., (83)].
The movements corresponding to F and Er were virtually constant at all velocities, whereas Ez + Es changed dramatically with speed [cf. Fig. 2, A-C, data from Goslow et al. (83)]. At each speed they found that the angles in each joint were very reproducible and that it was even possible to predict the angles in the other joints from the recordings of one joint; i.e., the limb behaved as one unity and the movements in the different joints were tightly coupled. Concerning the amplitude of changes in joint angles (in F, El, Ez, E3) at different speeds unfortunately no detailed data are available. The step length (i.e., step duration X velocity) increases linearly with speed. The so-called step length is composed of two parts: a) the distance the animal travels during the swing phase, which must increase linearly with velocity, since the swing time is constant; 6) the distance traveled during each stance phase (i.e., the important part), which is almost constant (11) [for cat 30-35 cm (99)] and independent of the speed (walk or trot, Fig. 20 from dog). This implies that the hip joint angles traversed during the stance phase should be rather constant and independent of the speed, which at least is not contradicted by the kinematic material (67, 83). The hip joint angles traversed during stance appear constant also in the gallop but the distance the animal can travel during each stance appears then somewhat prolonged by flexion and extension of the lower spine (83) (cf. Fig. 6). Many of the findings of Arshavsky et al. (11) were confirmed for the freely walking cat in a much more detailed study by Goslow et al. (83), which also contains a lot of useful information concerning speed and amplitude of the muscle movements during locomotion (cf. also 162). In conclusion, as the speed of locomotion increases, the number of step cycles per second increases markedly. The corresponding reduction in cycle duration is almost exclusively due to a shortening of the extension phase, whereas the flexion is kept nearly constant. The propulsive force obviously can act only during the stance phase, which is long during a slow walk but very short in a fast gallop (65 ms in Fig. 2). During rapid progression the propulsive force thus must be during a very brief’ period of time. This force is contributed by the dif“injected” ferent hip extensors as well as the intrinsic limb muscles extending after the yield
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April
197.5
CONTROL
OF
I,OCORtfOTION
251
(see below). The period during which the limb is in contact with ground seems. prolonged at higher speeds (gallop) due to the movements of the lower spine. Thereby the animal can travel longer in each contact period (i.e., has higher speed) than it could with only movements of the hip. This results in a larger horizc.ntal impulse (force X time). The fact that the duration of the stance phase must shorten with increasing speed is clear if one considers only the mechanical design of the limbs and everyday experience of how an animal ambulates. The relevant parameter to discuss is rather the propulsive force or impulse contributed during each step cycle at different speeds and to state that with a certain force the stance phase will be of a certain duration and the animal at steady state will move at a certain speed. With a higher horizontal impulse the animal can move faster, which leads to a shorter stance, however. To test the stability of the individual phases of the step cycle Orlovsky and Shik (191) perturbed the movements in the elbow joint by fixing over this joint a device by which a braking force could be applied by an electromagnetic clutch. If a braking force was applied throughout the flexion phase the movements were delayed by 30 ms or so but the final amplitude was close to normal. If, on the other hand, the braking force was applied during El and Ea the amplitude of the movements in El was markedly reduced and the elbow remained too flexed throughout Ez. They concluded that the F phase was very stable whereas El and Ez were much more sensitive to external perturbations. Two factors might contribute to the relative stability of F: one is the servoassistance brought about by the y-loop (165, 241) and another the building up of contractile activity during the shortlasting F ( 100-l 30 ms), which might in itself act to overcome an increased load. The mechanical situation is different during El. If the elbow is considered analogous to the knee it can be stated that a large part of the extension in El is brought about by passive factors (inertia), and it is noteworthy that the electromyogram (EMG) activity is rather small and starts after the onset of El. Hence it cannot be expected that the joint angles in the knee would approach normal levels and neither that EZ would be normal since it is in itself due to passive factors (205). B. E/ectromvogruphy The EMG activity of individual hindlimb muscles during locomotion has been studied in the cat by Engberg and Lundberg (65-67) and in the dog by Tomita (271). Th e main results are summarized in Fig. 3. The extensor muscles with a large increase in the start with a small activity in early El and continue before the foot makes contact with ground, which excludes later part of El-i.e., any possible reflex contribution from the toe pads in eliciting the muscle activity in the stance phase. The duration of the extensor EMG is dependent on the speed of locomotion. It stops generally some 4-O-50 ms before the foot leaves ground, which of course means that a lot of residual tension will remain in the extensor muscles until the end of the stance phase. In addition the short dorsiflexors of the toes are active throughout the extension phase but with their main activity in El
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252
Volume 55
S. GRILLNER
t
F
.E,
4E2.
E3
AM
hip
Q
knee
G
ankle
FDL
toe
FDB
toe
EDB
ext.
toe
EDL
lz
toe
TA
Ez
ankle
St
Ez
knee
fzz
hip
IP
I -
swing +
flexionl-
-
flex. !
stance +
extension
phase -+
3. Schelnatic representation of electromyographic activity of sollie hindlimb during locomotion. Hatched areas indicate part of step cycle in which muscles S c h eme is based largely on the data of Engberg and Lundberg (65, 66). Their A scheme like this can thus only indicate by recording one muscle at a time.
FIG.
the cat ‘(EMG). collected approximate particular
manner the precise muscles some uncertainty
of their illustrations a comparison with
shows activity the mesencephalic
relationship between exact onset of different on cessation of activity was present. First, for
a large part preparation
muscles of are active data were in a rather
muscles. for iliopsoas
For
2 one
of El, whereas in another it is not present. Here (see below) suggested that as a rule the activity
ceases earlier, which also indicates that the activity in EDL and TA is very similar. For extensors (particularly Q) many of their records show, instead of a low level of activity in the larger part of E1 followed by a marked increase in late El, a little burst in the 1st part of El followed by decreased of activity can be seen intermingled activity and subsequent strong activity in late E 1. The 2 types AhT, adductor magnus; Q, quadriceps; G, when activity in the mesencephalic cat is recorded. FDB, flexor digitoruin brevis; EDB, extensor gastrocnemius ; FDL, flexor digitoruIn longus; digitorum
brevis
; EDL,
extensor
digitorum
longus;
T;\,
tibialis
anterior;
iliopsoas. On right is indicated cation is made in physiological cides with the extensor, but
at which joint the relevant muscle is a prime EDB is not classified flexors and extensors. it is a dorsiflexor of the toes and for other reasons
as a flexor
(224).
by
Sherrington
St, semitendinosus;
Ip,
mover and a classifisince its activity coinit has been
classified
and Ez. This cocontraction of flexors and extensors of the foot is presumably due to the need for precise placing of the foot on ground. The flexor muscles start their activity in the later part of Es and are active through the larger part of F with the exception of the posterior knee flexors (semitendinosus, gracilis, and posterior biceps), which stop their activity in early F. This is presumably due to their anatomical insertion to the ischiatic tuberosity and the tibia, resulting in a double joint action of knee flexion and hip extension that is significant only when the hip is in a flexed position (224). An activity in the knee flexors in the later part of F to nate thus would actually counteract the hip flexion. It therefore is important that the medial sartorius, which flexes both hip and knee, has a more long-lasting that the knee flexors activity than the other knee flexors. It is also noteworthy have a short burst of activity in El-Ez, particularly during faster movements, which in all likelihood would contribute to the first part of the hip extension. Some double joint muscles not represented here in this scheme (Fig. 3) have more com-
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April
1975
CONTROL
OF
LOCOMOTION
253
plex and variable patterns with bursts of activity in both F and Er that might be speed dependent (67). For the forelimb no information is available on the cat, whereas in the dog a similar type of alternating activity has been recorded (271). Quantitative aspects of how the degree of muscle activation changes (increases), with speed are hardly known. It has been noted from studies with integrated EMG that the general level of activity increases at least in flexors (67) (cf. sect. IIC). In mesencephalic locomotion (cat, see sect. IVA) it has been shown that there is a progressive recruitment of new motor units with increasing speed and little effect on the frequency of the motor units already active at lower speeds (220). A somewhat similar EMG pattern is found in walking man with an alternate pattern with cocontractions in some muscles (46, in flexors and extensors but in addition is that, in contrast to the other extensors of the 59, 60). One notable exception hindlimb, the ankle extensors show no significant activity until the middle part of the stance phase. When considering that during walking the heel strikes the ground first, it is evident that a marked activity in ankle extensors would counteract the movement and it is only when the heel leaves the ground in the midstance that an ankle extensor activity is needed. On the other hand, during running, when humans use forefoot support, the EMG activity in the ankle extensors starts prior to foot contact with the ground (Grillner and Rossignol, unpublished observations). It is apparent that the ankle extensors must develop force to counteract the weight of the body before foot contact. During initiation of locomotion a complex interaction of different muscles occurs that recently has been described in detail by Herman et al. (119). The EMG activity in the forelimb of the newt (urodele) is more complex and, although a main scheme of alternate activity can be distinguished, cocontraction of various muscles is the rule and each muscle appears to have more of an individualized pattern [Szekely et al. (249)] than in the hindlimb of the cat. C. Forces It is apparent that a given amount of muscle activity can produce very different movements depending on dynamic and static conditions in the part of the body operated by this muscle. When a certain degree of muscle activity acts against an ongoing movement [e.g., Bernstein (28)] this might either reverse this movement or only result in a deceleration, whereas if it acts in the same direction It therefore is important to know which it might cause a marked acceleration. muscle contraction; passive, i.e., inertia) and which forces are acting (active, i.e., masses are involved in order to be able to predict what movements will occur from the activation of a muscle. High-speed cinematography or recording with accelerometers can reveal the size and direction of acceleration and velocity of the different parts of the body. If the masses of the different body segments are measured the forces acting on different parts of the body as well as on the center of gravity of the body and the torque acting at different joints can also be computed (28, 35, 57, 60, 64, 137, 160). Such work has been carried out on humans and to a rather limited extent on
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254
S. GRILLNER
Volume
55
animals. A wealth of biomechanical data of this type exists but so far very little work has been carried out on how these different parameters change with speed. The speed with which the hindlimb of the cat is brought backward in relation to the body increases with the velocity of the cat but the speed with which it is brought forward again is kept remarkably constant (F phase of constant duration). This must mean that the inertia to be overcome at the transition from extension to flexion must also increase with speed. It is of mechanical advantage that flexion occurs in knee, ankle, and hip because this brings the mass as close to the pivot as possible and thus the force required is reduced. The speed of the limb (F) in relation to the body (see above) should be approximately constant at different forward velocities in the last part of F and therefore the moment of inertia in relation to the body is kept largely constant. This moment of inertia will tend to continue the limb’s forward movement in relation to the body. Consequently even if the active flexor contribution (EMG) ceases the forward movement will whereas the same moment of intend to continue (i.e., a hip flexion continues), ertia will open up the knee (and ankle) and thereby initiate El in the knee. It is noteworthy that the EMG activity in all extensor muscles starts well after the onset of El and the activity is rather small until the period just preceding foot contact, when it increases to a high level (the activation pattern of double joint muscles, however, is unclear). The characteristic lag between onset of extension in knee and ankle versus hip (Fig. 1) is in all likelihood mainly or entirely due to passive factors and the extensor activation (EMG) causes the onset of hip extension as well as an active contraction of knee and ankle muscles. Information regarding forces during the stance phase can also be obtained by the use of force plates on the ground (14, 15, 64, 160) on which the foot is placed during locomotion (shown for cat in Fig. 4A). The horizontal force is negative during the first part of the step and actually counteracts the ongoing movements, whereas later in the cycle the body is pushed forward again. For humans it has been shown that the horizontal negative and positive forces both increase linearly with speed, but that the positive force always exceeds the negative by approximately 20 % (Wirta, unpublished observations). The vertical forces are more homogenous and reproducible (14, 15, 59, 60, 64, 160) (Fig. 4A). From such data (160) the total muscle force at each instant in the stance can be estimated. When the direction and size of the mechanical axis, the point of support, and the angles in the different joints of the limb investigated are known, the distance between the mechanical axis and the different joints allows a calculation of the torque acting at the individual joints during the support phase. The forces producing this torque can be calculated if also the origin and insertion of the relevant muscle and the size of the lever arms are considered (102, 104). It should first be noted that the muscle force required for obtaining a given torque varies drastically with the joint angle (Fig. 4B). For the ankle of the cat the joint angles between 70 and 120” require the minimal force but outside this region the force needed increases steeply. During locomotion and standing this favorable range (70-120”) is usually employed (56, 67, 83, 160). The force developed in the ankle extensors during a slow walk was calculated as outlined above by Grillner
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April
CONTROL
2975
OF
255
LOCOMOTION
hindlimb
constant
400
ms
120”
90”
angle
C
torque
60’
30”
of the ankle
D
force 0 angle x
4 (“1 ^a3 -x E p2
I
125 t oslset of stance phase
0
250
375
ms
1:5O angle
I;O” of the ankle
kl”
FIG. 4. Forces of hindlimb against ground and of ankle extensors during locomotion. A: horizontal and vertical force developed during stance phase of a slow walk during locomotion [from R’Ianter (160)]. B: force required in ankle extensors to produce a constant torque around ankle at different joint angles. Two different torque values are illustrated. Gradually increasing
line shows muscle steep range, which
stiffness coincides
of soleus with
at different that of joint
mated force development in ankle extensors ankle. D: data of C replotted as force versus joint angle corresponding to largest muscle
joint angles (soleus activated angles normally used during
in different parts of step cycle joint angle. Note that largest length [replotted from Grillner
at 20 Hz). locomotion.
Note
very C: esti-
and also joint angles in force is produced at a (104)].
(104) from Manter’s (160) force-plate measurements (Fig. 4, C, D). After the actively contracting ankle extensors are stretched and the maximal prcduced at the maximal length, i.e., the end of Ez. Thereafter the muscle and in parallel the force output decreases. The increase of force in Ez is
contact, force is shortens presum-
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256
S. GIULLNEK
Volume
55
ably produced in two ways: I) the motor units recruited in the beginning of the stance are still building up force due to the summation resulting from the repeated activation of the units; 2) as the muscle lengthens the contracting motor units will move up their length-tension curves and indeed the length-tension curve is very steep at the joint angles used in locomotion (cf. Fig. 4B and refs 102, 104, and 142). It can be assumed that the muscle properties will contribute substantially in load compensation during locomotion (102, 104). This has the advantage of occurring without lag (206), contrary to the inevitable lags of the stretch reflex, for instance, which can induce a detectable change of tension after only 20 ms (176). It can be assumed that in the cat passive factors like ligaments and fascias are not influencing the total force development in, for example, the normal range of ankle movements but outside this range they can be quite significant and help to compensate a very sudden extra load. It should be noted that this contribution in the ankle is dependent on the angle of the knee and set by the gastrocnemius fascias [Grillner (102, 104); Forssberg, unpublished observations]. In the horse, nature has explored purely passive factors in that the “metatarso-phalangeal” joint is supported mainly by the elastic “spring-ligament” (122). Another important aspect relates to the fact that the contracting muscles are stretched in E, prior to their shortening. A contraction during shortening will produce significantly more tension if the muscle has just been lengthened actively than if it shortens from isometric conditions (22, 47, 48a, 48b, 49; cf. 83). This extra force seems to occur without increased energy expenditure by the muscles and thus is not only effective in producing tension but also economical. This means that it might be more relevant to regard the stance phase (i.e., E2 + E3) as one unity, a stretch-shortening cycle (83).
III.
MOVEMENTS
OF
ENTIRE
ANIMAL
: INTERLIMB
COORDINATIOK
During ambulation the four limbs of a tetrapod have to be moved in such a manner that they can jointly provide the suitable forward force at a minimal energy expenditure. This must be carried out with a maintained equilibrium; i.e., the projection of the center of gravity must fall in an optimally stable point between the moving points of support. Equilibrium control is relatively simple for amphibians and reptiles, which have their points of support as lateral as possible with the humerus and femur pointing laterally and only the lower parts of the limbs being vertical and supporting the body. With the more refined nervous system of mammals it has been possible to move the limbs to a vertical position under the point of origin on shoulder or pelvis. Many advantages thus have been gained for speed and agility of the locomotion, but more severe problems have been imposed on the equilibrium control system. For equilibrium stability the order in which the limbs are put down on the ground is important and it is striking that one sequence is typical for vertebrates -i.e., the footfall of left hindlimb (LH) precedes left forelimb (LF), which is followed by right hindlimb (RH) and right forelimb (RF) (Fig. 5). This applies
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April
197.5 FIG.
tion
during
CONTROL
5. Interlimb walk and
Periods of foot contact for 1 step cycle starting
are plotted with foot
forelimb. Below contact of each limb is plotted phase in which limb is put down in relation to
divided by duration cycle). [Replotted at. (247).]
257
LOCOMOTION
coordinatrot (cat).
strike of left hindlimb (LH). Bars indicate period of contact. LF, RH, and RF indicate left forelimb, right hindlimb, and
step cycle of LH onset of step cycle
OF
(i.e., time frorn to foot contact
walk
LH LF ,-+,
j
trot I,28 m/s
m/s
~~~~~~~
RF @
036
c 0
0,25
0,50
0,75
I 200ms
4
I,0
0
0,5
40 ;OOms
of entire step from Stuart et
to amphibians, reptiles, and walking and tro tting mam mals. From a mechan ical point of view Gray (87, 90) has pointed out the great advantage gained by this gives a turning couple that, if not countersequence (hind -+ fore). The hindlimb acted by the forelimbs, would make the front part rotate around a transverse axis through the body and thereby the front part would be rotated toward ground. This would be a problem if the hindlimbs were allowed to operate alone, but this will not be the case since the forelimbs are always the last to leave the ground. In other words the locomotor program is adapted to provide optimal stability. The pairs of limbs at the hip and shoulder girdles are coordinated in principle in two ways. 1) In strict alternation the two legs of one pair are 0.5 out of phase (i.e., if one limb strikes the ground at zero, the other limb will strike ground only after half the cycle of the first limb is completed). This occurs during walk, trot, and pace (Fig. 5) and corresponds to the symmetrical gaits [cf. Howell (133)]. 2) The limbs of one girdle work in phase with each other so that they extend and flex almost simultaneously, i.e., in-phase coordination. Often one limb of a pair strikes ground somewhat before the other in the order of 0.1-0.2 out of phase. These arc the difierent forms of gallop and leaping (Figs. 6 and 7). The expression in phase was coined by Miller et al. (172) and corresponds to the asymmetrical gaits described by Howell (133), for example. Terms for the different types of gait exist in the common language and they were described long ago in quite some detail (163, 204). With the technique of photography new possibilities opened up for a systematic analysis, and the American photographer Muybridge (175) designed a way of triggering a number of cameras in succession and thereby could get detailed sequential data on each type of gait. He depicted locomotion under many different conditions in a variety of animals, e.g., horses, walking and trotting sows, cats, dogs, lions, antelopes, raccoons, eagles, and kangaroos. He presented the different gaits in so-called footfall patterns, which informs one about the sequence in which the feet make contact with and leave the ground. Such schemes have been used particularly for mammals for a very long time (90, 133, 214) but unfortunately give no information regarding the absolute and relative duration of the different phases. Much more detailed
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258
S. GRILLNER
jj T -------------_---------h
I I
I
I I
I
1;
iJ
-m---m----
--------s----I
LH LF RH RF FIG.
rnents period
--
--
6. Longitudinal
of newt. of foot
lateral from
---+I ---~---------b&-------b-4----.--
body Gray
Note contact
movements @O)].
A transverse
body
--+j------
6
--
-t--+------+4,
(
movement
flexion and extension for galloping cheetah of walking
----. -.-----
newt.
----..-----~------
for
horse
and
cheetah
during
of lower spine for horse and [redrawn from Hildebrand Note
how
these
gallop cheetah. (12 l)].
movements
prolong
and
lateral
move-
Below is indicated To right is shown the
step
[redrawn
C
5.6 m/s
7. Pattern during different Abbreviations
FIG.
tacts gallop.
of foot contypes of same as in
Fig. 5. [Replotted from Stuart et al. (247); half bound to right is slightly modified from their
graph*1 100 ms
information is needed to understand the structure of the gait and the time lags involved. It is likely that even today our knowledge concerning interlimb coordination would be enlarged, if the sequences depicted so beautifully a century ago by Muybridge were analyzed. Marey (161, 162) and Hildebrand (12 1, 123, 124) represented such data in the form of diagrams such as Fig. 5. This gives much more information, and still more is contained in the analysis of Arshavsky et al. (1 l), Miller and Van Der Burg (172), and Stuart et al. (247), who improved the description of gait patterns by taking into consideration not only transfer and support but also flexion and extension. The different types of alternate gaits can be described as follows: I) In the walk the limbs strike ground in the order LH, LF, RH, RF. In the
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A@
1975
CONTROL
OF
LOCOMOTION
259
idealized form there is 0.25 of a cycle in between each foot strike, i.e., the forelimb strikes the ground in p + 0.25 in the cycle starting with contact of the ipsilateral hindlimb (Fig. 5A). H owever, this phase value seems to vary with speed (see below). Since the swing phase for each limb is approximately constant at all speeds, whereas the stance phase changes considerably (cf. above), it is apparent that at very slow speeds of walking three or four limbs can alternately support the cat during progression. As the speed increases fewer limbs can support the body simultaneously and in a running walk alternately one and two limbs support the body at the same time. A running walk is called the rack by some authors (123) and the amble or fox trot by others. 2) In the trot the two diagonal limbs work synchronously and hence the forelimb strikes in p + 0.5 of the ipsilateral hindlimb (Fig. 5B). 3) In the puce the ipsilateral limbs are synchronous, i.e.
PHYSIOLOGICAL
Vol.
55, No. 2, April 1975 Printed in U.S. A.
Locomotion Mechanisms
Central
in Vertebrates: and Reflex Interaction
S. GRILLNER Department I. II.
IV. V.
VI.
VII.
IX. X.
I.
of Giiteborg,
Gb’teborg,
Sweden 247 248 248
Electromyography...............................................
C. Forces. ........................................................ Movements of Entire Animal : Interlimb Coordination. A. In-phase gaits. .................................................. B. Comparative aspects of locomotion. ................................ C. How is interlimb coordination achieved in D. Bipedal locomotion. ............................................. Locomotion in Decorticate and Mesencephalic A. Locomotion Deafferentation mechanisms
in acute high experiments .........
...................
Preparations
259 260 262
C. D. E.
Mammals. ..................................................... Fishes. ......................................................... Comments and conclusions. ......................................
265 266 267
..............
decerebrate cats. ......................... and other evidence for central ........................................
Amphibians. Reptiles
and
251 253 256
tetrapods? ..................
A. B.
locomotor 272 272
.................................................... birds. ..............................................
273 274 275 276 277 277 279
Locomotor Capacity of Spinal Cord. .................................. A Fishes and lower chordates. ....................................... B. Amphibians ..................................................... C. Reptiles and birds. .............................................. D. Mammals Central Pattern A. B.
VIII.
University
Introduction ....................................................... Step Cycle of the Individual Limb. ................................... ~2. Kinematics. .................................................... B.
I I I.
of Physiology,
Brown’s Neuronal
...................................................... Generator for Locomotion
.............................
Significance .A. Peripheral B. Systems C. Possible
and its development. ............................ possibly related to generation of locomotion. ......... ........................ of Peripheral Input in Locomotion. inputs influencing step cycle and gait. .................... taking part in autoregulation of muscle activity. .............. phasic control of reflex arcs related to step-cycle reflex reversals.
D. Reflexes Descending A. Descending
that have been related to locomotion: negative findings. ....... Control of Spinal Locomotion Circuitry. ..................... systems possibly responsible for tonic activation. ...........
Concluding
279 280 282 284 285
hypothesis activity
Remarks
...............................................
287 288 290 ..
290 291 293 294 295
INTRODUCTION
During ambulation an animal has to deal with at least three different tasks. I) It must perform the actual locomotor movements of the different limbs according to a rather stereotyped plan. 2) It must adapt these movements to external condi247
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248
S. GRILLNER
Volume
55
tions in order to accomplish purposeful locomotion so as to achieve various goals such as catching prey or escaping an enemy. Furthermore in almost each step cycle adjustments must be made to place the limb properly, e.g., on a stone and not in a hole; i.e., the animal must continously anticipate where to put down the foot. 3) It must maintain equilibrium during the movements; i.e., the projection of the center of gravity must fall in an optimally stable point between the moving points of support and be maintained within rather narrow limits. In order to accomplish this a whole set of different compensating mechanisms has evolved that enables the animal to counteract various types of unexpected perturbations. This review deals almost exclusively with the first task-i.e., how does the central nervous system generate the actual locomotor movements. I have attempted to compare the different classes of vertebrates in order to extract the common features that emerge. It is natural that some pertinent work might have been excluded, since it is possible only to cover some general aspects and approaches, i.e., those that the reviewer at present has felt as the most important. Flight in vertebrates has not been considered but the reader is referred to the interesting review of Pennycuick (197) for the mechanical aspects of flight. In order to have any reasonable chance to understand the underlying nervous mechanisms, we must first know what movements are actually perf’ormed by the individual limbs and how the limbs are coordinated. Which factors change at different speeds and which factors remain constant? What are the time constraints, the forces, and the contribution of individual muscles? Therefore this type of basic information is considered first in order to be able to later consider central mechanisms.
II.
STEP
CYCLE
OF
THE
INDIVIDUAL
LIMB
A. Kinematics The limbs serve two purposes during locomotion: to support the body during the ongoing movement as the wheels of a carriage and to generate the propulsive force for progession to take place. The actual locomotor movements were analyzed cinematographically by Philippson (205), who measured how the different jcint angles change with time (see Fig. 1). Just after the foot leaves the ground a flexion occurring in knee, ankle, and hip brings the limb forward to a more rostra1 postion [i.e., the flexion phase (F)], where the knee and ankle start to extend and somewhat later the hip [i.e., the start of the extension phase (E)]. This phase is divided into three parts: Er, during which the limb is extended and brought down to contact with ground; Ez, when the knee and ankle flex somewhat, yielding under the weight of the body after contact; E 3, during which the limb extends again and This classification scheme has been used by many pushes the animal forward. subsequent authors (66, 67, 83, 160), but other terms are frequently used (see Fig. 1). It should be noted that the foot is in contact with the ground only in EZ and Es (stance or support phase) and is off the ground in F and Er (swing or
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April
1975
CONTROL
OF
249
LOCOMOTION
transfer phase). Flexion and protraction are often used as synonyms as well as retraction and extension (Fig. 1). Some authors utilize this terminology when describing particularly the hip movement, which differs from that of the knee. The E2 phase appears to be purely passive since during stepping movements in the air only one single extension movement occurs (205). Thus when the limb does not have to carry the weight under which it yields, no ET is found. The same is true during movement in another homogeneous medium such as swimming in water (172). The cat always uses the forefoot as support (digitigrade), whereas other animals such as the bear or humans put down their heels first in walking (plantigrade support). It is interesting that during running there is a shift to digitigrade locomotion. The leg movements are similar in principle (28, 16 1, 162) in both cases and the Philippson step cycle has been applied to humans (119). The limb movements for amphibians and reptiles, though not as well studied, are considered further below (interlimb coordination). They differ fundamentally in that the femur and humerus point laterally and the movement of the limb is similar to that of a spoke of a horizontal wheel being brought back and forth (90). Arshavsky et al. (11) studied the step cycle of fore- and hindlimbs in order to quantify the step-cycle changes with the speed of locomotion and to determine if certain parts of the cycle would be constant and others speed dependent (dogs). The animals walked on a treadmill that could be set at different constant velocities. walk
0.6 m/s
gallop
0I
150 130 -
XX
XX
X
7.3 m/s
150 130
0 ;
II0
I
0
I IO
.x
Lo,
I k E
.-
90
.-0
70
11 :F:E, I 8 :flexion: + : pro- :+--, I :4- swing ++: +-transfer++
FIG.
slow
walk
90
0
X’ x
;y2: ’ extension retraction
hatched region. walk and gallop, of step cycle are
limb is drawn for account movement
x hip l ankle
70
I I I
stance
,
support
1. Step cycle. Joint angles and a fast gallop [replotted
is indicated by phase) between different phases
E3
I
in ankle and from Goslow
hip are plotted throughout et al. (83)]. Below graphs
one period
Note striking difference in duration of contact whereas swing phase remains constant. Different listed below graph. Under right graph approximate
the different phases indicated of lower spine (see text).
by interrupted
lines.
Drawings
step cycle in a of foot contact period terms do not
(stance used for position of take
into
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250
S. GKILLNEK
Volume
55
B 200
L F
IO0
El
0
2
4
velocity FIG.
swing which
0
in step
at different marked
24
velocity
(m/s)
2. Changes
and stance is particularly
6
cycle
with
0
6
(m/s)
different
2
4
velocity forward
velocities
forward velocities. Note marked for ES (shown in C). Swing phase
6
0
I234 velocity
(m/s) of locomotion.
(rds)
A; duration
of
speed dependence of stance phase, is virtually constant; although El
varies somewhat, F is constant (shown in H). D: step length is plotted (i.e., total step-cycle tion X velocity) at different speeds and below is distance traveled during each stance phase duration of stance X velocity). A-C are from the cat [replotted from Goslow et al. phase D is from the dog [from Arshavsky et al. (1 l)].
dura(i.e., (83)].
The movements corresponding to F and Er were virtually constant at all velocities, whereas Ez + Es changed dramatically with speed [cf. Fig. 2, A-C, data from Goslow et al. (83)]. At each speed they found that the angles in each joint were very reproducible and that it was even possible to predict the angles in the other joints from the recordings of one joint; i.e., the limb behaved as one unity and the movements in the different joints were tightly coupled. Concerning the amplitude of changes in joint angles (in F, El, Ez, E3) at different speeds unfortunately no detailed data are available. The step length (i.e., step duration X velocity) increases linearly with speed. The so-called step length is composed of two parts: a) the distance the animal travels during the swing phase, which must increase linearly with velocity, since the swing time is constant; 6) the distance traveled during each stance phase (i.e., the important part), which is almost constant (11) [for cat 30-35 cm (99)] and independent of the speed (walk or trot, Fig. 20 from dog). This implies that the hip joint angles traversed during the stance phase should be rather constant and independent of the speed, which at least is not contradicted by the kinematic material (67, 83). The hip joint angles traversed during stance appear constant also in the gallop but the distance the animal can travel during each stance appears then somewhat prolonged by flexion and extension of the lower spine (83) (cf. Fig. 6). Many of the findings of Arshavsky et al. (11) were confirmed for the freely walking cat in a much more detailed study by Goslow et al. (83), which also contains a lot of useful information concerning speed and amplitude of the muscle movements during locomotion (cf. also 162). In conclusion, as the speed of locomotion increases, the number of step cycles per second increases markedly. The corresponding reduction in cycle duration is almost exclusively due to a shortening of the extension phase, whereas the flexion is kept nearly constant. The propulsive force obviously can act only during the stance phase, which is long during a slow walk but very short in a fast gallop (65 ms in Fig. 2). During rapid progression the propulsive force thus must be during a very brief’ period of time. This force is contributed by the dif“injected” ferent hip extensors as well as the intrinsic limb muscles extending after the yield
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April
197.5
CONTROL
OF
I,OCORtfOTION
251
(see below). The period during which the limb is in contact with ground seems. prolonged at higher speeds (gallop) due to the movements of the lower spine. Thereby the animal can travel longer in each contact period (i.e., has higher speed) than it could with only movements of the hip. This results in a larger horizc.ntal impulse (force X time). The fact that the duration of the stance phase must shorten with increasing speed is clear if one considers only the mechanical design of the limbs and everyday experience of how an animal ambulates. The relevant parameter to discuss is rather the propulsive force or impulse contributed during each step cycle at different speeds and to state that with a certain force the stance phase will be of a certain duration and the animal at steady state will move at a certain speed. With a higher horizontal impulse the animal can move faster, which leads to a shorter stance, however. To test the stability of the individual phases of the step cycle Orlovsky and Shik (191) perturbed the movements in the elbow joint by fixing over this joint a device by which a braking force could be applied by an electromagnetic clutch. If a braking force was applied throughout the flexion phase the movements were delayed by 30 ms or so but the final amplitude was close to normal. If, on the other hand, the braking force was applied during El and Ea the amplitude of the movements in El was markedly reduced and the elbow remained too flexed throughout Ez. They concluded that the F phase was very stable whereas El and Ez were much more sensitive to external perturbations. Two factors might contribute to the relative stability of F: one is the servoassistance brought about by the y-loop (165, 241) and another the building up of contractile activity during the shortlasting F ( 100-l 30 ms), which might in itself act to overcome an increased load. The mechanical situation is different during El. If the elbow is considered analogous to the knee it can be stated that a large part of the extension in El is brought about by passive factors (inertia), and it is noteworthy that the electromyogram (EMG) activity is rather small and starts after the onset of El. Hence it cannot be expected that the joint angles in the knee would approach normal levels and neither that EZ would be normal since it is in itself due to passive factors (205). B. E/ectromvogruphy The EMG activity of individual hindlimb muscles during locomotion has been studied in the cat by Engberg and Lundberg (65-67) and in the dog by Tomita (271). Th e main results are summarized in Fig. 3. The extensor muscles with a large increase in the start with a small activity in early El and continue before the foot makes contact with ground, which excludes later part of El-i.e., any possible reflex contribution from the toe pads in eliciting the muscle activity in the stance phase. The duration of the extensor EMG is dependent on the speed of locomotion. It stops generally some 4-O-50 ms before the foot leaves ground, which of course means that a lot of residual tension will remain in the extensor muscles until the end of the stance phase. In addition the short dorsiflexors of the toes are active throughout the extension phase but with their main activity in El
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252
Volume 55
S. GRILLNER
t
F
.E,
4E2.
E3
AM
hip
Q
knee
G
ankle
FDL
toe
FDB
toe
EDB
ext.
toe
EDL
lz
toe
TA
Ez
ankle
St
Ez
knee
fzz
hip
IP
I -
swing +
flexionl-
-
flex. !
stance +
extension
phase -+
3. Schelnatic representation of electromyographic activity of sollie hindlimb during locomotion. Hatched areas indicate part of step cycle in which muscles S c h eme is based largely on the data of Engberg and Lundberg (65, 66). Their A scheme like this can thus only indicate by recording one muscle at a time.
FIG.
the cat ‘(EMG). collected approximate particular
manner the precise muscles some uncertainty
of their illustrations a comparison with
shows activity the mesencephalic
relationship between exact onset of different on cessation of activity was present. First, for
a large part preparation
muscles of are active data were in a rather
muscles. for iliopsoas
For
2 one
of El, whereas in another it is not present. Here (see below) suggested that as a rule the activity
ceases earlier, which also indicates that the activity in EDL and TA is very similar. For extensors (particularly Q) many of their records show, instead of a low level of activity in the larger part of E1 followed by a marked increase in late El, a little burst in the 1st part of El followed by decreased of activity can be seen intermingled activity and subsequent strong activity in late E 1. The 2 types AhT, adductor magnus; Q, quadriceps; G, when activity in the mesencephalic cat is recorded. FDB, flexor digitoruin brevis; EDB, extensor gastrocnemius ; FDL, flexor digitoruIn longus; digitorum
brevis
; EDL,
extensor
digitorum
longus;
T;\,
tibialis
anterior;
iliopsoas. On right is indicated cation is made in physiological cides with the extensor, but
at which joint the relevant muscle is a prime EDB is not classified flexors and extensors. it is a dorsiflexor of the toes and for other reasons
as a flexor
(224).
by
Sherrington
St, semitendinosus;
Ip,
mover and a classifisince its activity coinit has been
classified
and Ez. This cocontraction of flexors and extensors of the foot is presumably due to the need for precise placing of the foot on ground. The flexor muscles start their activity in the later part of Es and are active through the larger part of F with the exception of the posterior knee flexors (semitendinosus, gracilis, and posterior biceps), which stop their activity in early F. This is presumably due to their anatomical insertion to the ischiatic tuberosity and the tibia, resulting in a double joint action of knee flexion and hip extension that is significant only when the hip is in a flexed position (224). An activity in the knee flexors in the later part of F to nate thus would actually counteract the hip flexion. It therefore is important that the medial sartorius, which flexes both hip and knee, has a more long-lasting that the knee flexors activity than the other knee flexors. It is also noteworthy have a short burst of activity in El-Ez, particularly during faster movements, which in all likelihood would contribute to the first part of the hip extension. Some double joint muscles not represented here in this scheme (Fig. 3) have more com-
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April
1975
CONTROL
OF
LOCOMOTION
253
plex and variable patterns with bursts of activity in both F and Er that might be speed dependent (67). For the forelimb no information is available on the cat, whereas in the dog a similar type of alternating activity has been recorded (271). Quantitative aspects of how the degree of muscle activation changes (increases), with speed are hardly known. It has been noted from studies with integrated EMG that the general level of activity increases at least in flexors (67) (cf. sect. IIC). In mesencephalic locomotion (cat, see sect. IVA) it has been shown that there is a progressive recruitment of new motor units with increasing speed and little effect on the frequency of the motor units already active at lower speeds (220). A somewhat similar EMG pattern is found in walking man with an alternate pattern with cocontractions in some muscles (46, in flexors and extensors but in addition is that, in contrast to the other extensors of the 59, 60). One notable exception hindlimb, the ankle extensors show no significant activity until the middle part of the stance phase. When considering that during walking the heel strikes the ground first, it is evident that a marked activity in ankle extensors would counteract the movement and it is only when the heel leaves the ground in the midstance that an ankle extensor activity is needed. On the other hand, during running, when humans use forefoot support, the EMG activity in the ankle extensors starts prior to foot contact with the ground (Grillner and Rossignol, unpublished observations). It is apparent that the ankle extensors must develop force to counteract the weight of the body before foot contact. During initiation of locomotion a complex interaction of different muscles occurs that recently has been described in detail by Herman et al. (119). The EMG activity in the forelimb of the newt (urodele) is more complex and, although a main scheme of alternate activity can be distinguished, cocontraction of various muscles is the rule and each muscle appears to have more of an individualized pattern [Szekely et al. (249)] than in the hindlimb of the cat. C. Forces It is apparent that a given amount of muscle activity can produce very different movements depending on dynamic and static conditions in the part of the body operated by this muscle. When a certain degree of muscle activity acts against an ongoing movement [e.g., Bernstein (28)] this might either reverse this movement or only result in a deceleration, whereas if it acts in the same direction It therefore is important to know which it might cause a marked acceleration. muscle contraction; passive, i.e., inertia) and which forces are acting (active, i.e., masses are involved in order to be able to predict what movements will occur from the activation of a muscle. High-speed cinematography or recording with accelerometers can reveal the size and direction of acceleration and velocity of the different parts of the body. If the masses of the different body segments are measured the forces acting on different parts of the body as well as on the center of gravity of the body and the torque acting at different joints can also be computed (28, 35, 57, 60, 64, 137, 160). Such work has been carried out on humans and to a rather limited extent on
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254
S. GRILLNER
Volume
55
animals. A wealth of biomechanical data of this type exists but so far very little work has been carried out on how these different parameters change with speed. The speed with which the hindlimb of the cat is brought backward in relation to the body increases with the velocity of the cat but the speed with which it is brought forward again is kept remarkably constant (F phase of constant duration). This must mean that the inertia to be overcome at the transition from extension to flexion must also increase with speed. It is of mechanical advantage that flexion occurs in knee, ankle, and hip because this brings the mass as close to the pivot as possible and thus the force required is reduced. The speed of the limb (F) in relation to the body (see above) should be approximately constant at different forward velocities in the last part of F and therefore the moment of inertia in relation to the body is kept largely constant. This moment of inertia will tend to continue the limb’s forward movement in relation to the body. Consequently even if the active flexor contribution (EMG) ceases the forward movement will whereas the same moment of intend to continue (i.e., a hip flexion continues), ertia will open up the knee (and ankle) and thereby initiate El in the knee. It is noteworthy that the EMG activity in all extensor muscles starts well after the onset of El and the activity is rather small until the period just preceding foot contact, when it increases to a high level (the activation pattern of double joint muscles, however, is unclear). The characteristic lag between onset of extension in knee and ankle versus hip (Fig. 1) is in all likelihood mainly or entirely due to passive factors and the extensor activation (EMG) causes the onset of hip extension as well as an active contraction of knee and ankle muscles. Information regarding forces during the stance phase can also be obtained by the use of force plates on the ground (14, 15, 64, 160) on which the foot is placed during locomotion (shown for cat in Fig. 4A). The horizontal force is negative during the first part of the step and actually counteracts the ongoing movements, whereas later in the cycle the body is pushed forward again. For humans it has been shown that the horizontal negative and positive forces both increase linearly with speed, but that the positive force always exceeds the negative by approximately 20 % (Wirta, unpublished observations). The vertical forces are more homogenous and reproducible (14, 15, 59, 60, 64, 160) (Fig. 4A). From such data (160) the total muscle force at each instant in the stance can be estimated. When the direction and size of the mechanical axis, the point of support, and the angles in the different joints of the limb investigated are known, the distance between the mechanical axis and the different joints allows a calculation of the torque acting at the individual joints during the support phase. The forces producing this torque can be calculated if also the origin and insertion of the relevant muscle and the size of the lever arms are considered (102, 104). It should first be noted that the muscle force required for obtaining a given torque varies drastically with the joint angle (Fig. 4B). For the ankle of the cat the joint angles between 70 and 120” require the minimal force but outside this region the force needed increases steeply. During locomotion and standing this favorable range (70-120”) is usually employed (56, 67, 83, 160). The force developed in the ankle extensors during a slow walk was calculated as outlined above by Grillner
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April
CONTROL
2975
OF
255
LOCOMOTION
hindlimb
constant
400
ms
120”
90”
angle
C
torque
60’
30”
of the ankle
D
force 0 angle x
4 (“1 ^a3 -x E p2
I
125 t oslset of stance phase
0
250
375
ms
1:5O angle
I;O” of the ankle
kl”
FIG. 4. Forces of hindlimb against ground and of ankle extensors during locomotion. A: horizontal and vertical force developed during stance phase of a slow walk during locomotion [from R’Ianter (160)]. B: force required in ankle extensors to produce a constant torque around ankle at different joint angles. Two different torque values are illustrated. Gradually increasing
line shows muscle steep range, which
stiffness coincides
of soleus with
at different that of joint
mated force development in ankle extensors ankle. D: data of C replotted as force versus joint angle corresponding to largest muscle
joint angles (soleus activated angles normally used during
in different parts of step cycle joint angle. Note that largest length [replotted from Grillner
at 20 Hz). locomotion.
Note
very C: esti-
and also joint angles in force is produced at a (104)].
(104) from Manter’s (160) force-plate measurements (Fig. 4, C, D). After the actively contracting ankle extensors are stretched and the maximal prcduced at the maximal length, i.e., the end of Ez. Thereafter the muscle and in parallel the force output decreases. The increase of force in Ez is
contact, force is shortens presum-
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256
S. GIULLNEK
Volume
55
ably produced in two ways: I) the motor units recruited in the beginning of the stance are still building up force due to the summation resulting from the repeated activation of the units; 2) as the muscle lengthens the contracting motor units will move up their length-tension curves and indeed the length-tension curve is very steep at the joint angles used in locomotion (cf. Fig. 4B and refs 102, 104, and 142). It can be assumed that the muscle properties will contribute substantially in load compensation during locomotion (102, 104). This has the advantage of occurring without lag (206), contrary to the inevitable lags of the stretch reflex, for instance, which can induce a detectable change of tension after only 20 ms (176). It can be assumed that in the cat passive factors like ligaments and fascias are not influencing the total force development in, for example, the normal range of ankle movements but outside this range they can be quite significant and help to compensate a very sudden extra load. It should be noted that this contribution in the ankle is dependent on the angle of the knee and set by the gastrocnemius fascias [Grillner (102, 104); Forssberg, unpublished observations]. In the horse, nature has explored purely passive factors in that the “metatarso-phalangeal” joint is supported mainly by the elastic “spring-ligament” (122). Another important aspect relates to the fact that the contracting muscles are stretched in E, prior to their shortening. A contraction during shortening will produce significantly more tension if the muscle has just been lengthened actively than if it shortens from isometric conditions (22, 47, 48a, 48b, 49; cf. 83). This extra force seems to occur without increased energy expenditure by the muscles and thus is not only effective in producing tension but also economical. This means that it might be more relevant to regard the stance phase (i.e., E2 + E3) as one unity, a stretch-shortening cycle (83).
III.
MOVEMENTS
OF
ENTIRE
ANIMAL
: INTERLIMB
COORDINATIOK
During ambulation the four limbs of a tetrapod have to be moved in such a manner that they can jointly provide the suitable forward force at a minimal energy expenditure. This must be carried out with a maintained equilibrium; i.e., the projection of the center of gravity must fall in an optimally stable point between the moving points of support. Equilibrium control is relatively simple for amphibians and reptiles, which have their points of support as lateral as possible with the humerus and femur pointing laterally and only the lower parts of the limbs being vertical and supporting the body. With the more refined nervous system of mammals it has been possible to move the limbs to a vertical position under the point of origin on shoulder or pelvis. Many advantages thus have been gained for speed and agility of the locomotion, but more severe problems have been imposed on the equilibrium control system. For equilibrium stability the order in which the limbs are put down on the ground is important and it is striking that one sequence is typical for vertebrates -i.e., the footfall of left hindlimb (LH) precedes left forelimb (LF), which is followed by right hindlimb (RH) and right forelimb (RF) (Fig. 5). This applies
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April
197.5 FIG.
tion
during
CONTROL
5. Interlimb walk and
Periods of foot contact for 1 step cycle starting
are plotted with foot
forelimb. Below contact of each limb is plotted phase in which limb is put down in relation to
divided by duration cycle). [Replotted at. (247).]
257
LOCOMOTION
coordinatrot (cat).
strike of left hindlimb (LH). Bars indicate period of contact. LF, RH, and RF indicate left forelimb, right hindlimb, and
step cycle of LH onset of step cycle
OF
(i.e., time frorn to foot contact
walk
LH LF ,-+,
j
trot I,28 m/s
m/s
~~~~~~~
RF @
036
c 0
0,25
0,50
0,75
I 200ms
4
I,0
0
0,5
40 ;OOms
of entire step from Stuart et
to amphibians, reptiles, and walking and tro tting mam mals. From a mechan ical point of view Gray (87, 90) has pointed out the great advantage gained by this gives a turning couple that, if not countersequence (hind -+ fore). The hindlimb acted by the forelimbs, would make the front part rotate around a transverse axis through the body and thereby the front part would be rotated toward ground. This would be a problem if the hindlimbs were allowed to operate alone, but this will not be the case since the forelimbs are always the last to leave the ground. In other words the locomotor program is adapted to provide optimal stability. The pairs of limbs at the hip and shoulder girdles are coordinated in principle in two ways. 1) In strict alternation the two legs of one pair are 0.5 out of phase (i.e., if one limb strikes the ground at zero, the other limb will strike ground only after half the cycle of the first limb is completed). This occurs during walk, trot, and pace (Fig. 5) and corresponds to the symmetrical gaits [cf. Howell (133)]. 2) The limbs of one girdle work in phase with each other so that they extend and flex almost simultaneously, i.e., in-phase coordination. Often one limb of a pair strikes ground somewhat before the other in the order of 0.1-0.2 out of phase. These arc the difierent forms of gallop and leaping (Figs. 6 and 7). The expression in phase was coined by Miller et al. (172) and corresponds to the asymmetrical gaits described by Howell (133), for example. Terms for the different types of gait exist in the common language and they were described long ago in quite some detail (163, 204). With the technique of photography new possibilities opened up for a systematic analysis, and the American photographer Muybridge (175) designed a way of triggering a number of cameras in succession and thereby could get detailed sequential data on each type of gait. He depicted locomotion under many different conditions in a variety of animals, e.g., horses, walking and trotting sows, cats, dogs, lions, antelopes, raccoons, eagles, and kangaroos. He presented the different gaits in so-called footfall patterns, which informs one about the sequence in which the feet make contact with and leave the ground. Such schemes have been used particularly for mammals for a very long time (90, 133, 214) but unfortunately give no information regarding the absolute and relative duration of the different phases. Much more detailed
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258
S. GRILLNER
jj T -------------_---------h
I I
I
I I
I
1;
iJ
-m---m----
--------s----I
LH LF RH RF FIG.
rnents period
--
--
6. Longitudinal
of newt. of foot
lateral from
---+I ---~---------b&-------b-4----.--
body Gray
Note contact
movements @O)].
A transverse
body
--+j------
6
--
-t--+------+4,
(
movement
flexion and extension for galloping cheetah of walking
----. -.-----
newt.
----..-----~------
for
horse
and
cheetah
during
of lower spine for horse and [redrawn from Hildebrand Note
how
these
gallop cheetah. (12 l)].
movements
prolong
and
lateral
move-
Below is indicated To right is shown the
step
[redrawn
C
5.6 m/s
7. Pattern during different Abbreviations
FIG.
tacts gallop.
of foot contypes of same as in
Fig. 5. [Replotted from Stuart et al. (247); half bound to right is slightly modified from their
graph*1 100 ms
information is needed to understand the structure of the gait and the time lags involved. It is likely that even today our knowledge concerning interlimb coordination would be enlarged, if the sequences depicted so beautifully a century ago by Muybridge were analyzed. Marey (161, 162) and Hildebrand (12 1, 123, 124) represented such data in the form of diagrams such as Fig. 5. This gives much more information, and still more is contained in the analysis of Arshavsky et al. (1 l), Miller and Van Der Burg (172), and Stuart et al. (247), who improved the description of gait patterns by taking into consideration not only transfer and support but also flexion and extension. The different types of alternate gaits can be described as follows: I) In the walk the limbs strike ground in the order LH, LF, RH, RF. In the
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A@
1975
CONTROL
OF
LOCOMOTION
259
idealized form there is 0.25 of a cycle in between each foot strike, i.e., the forelimb strikes the ground in p + 0.25 in the cycle starting with contact of the ipsilateral hindlimb (Fig. 5A). H owever, this phase value seems to vary with speed (see below). Since the swing phase for each limb is approximately constant at all speeds, whereas the stance phase changes considerably (cf. above), it is apparent that at very slow speeds of walking three or four limbs can alternately support the cat during progression. As the speed increases fewer limbs can support the body simultaneously and in a running walk alternately one and two limbs support the body at the same time. A running walk is called the rack by some authors (123) and the amble or fox trot by others. 2) In the trot the two diagonal limbs work synchronously and hence the forelimb strikes in p + 0.5 of the ipsilateral hindlimb (Fig. 5B). 3) In the puce the ipsilateral limbs are synchronous, i.e.
