Relationship between forelimb coordination and movement asymmetries during fast gaits, canter and gallop

352

Brain Research, 164 (I 979) 352-356

© Elsevier/North-HollandBiomedical Press

RelaUonship between forelimb coordination and movement ,asymmetries during fast gaits, canter and gallop

AVIS H. COHEN Section o f Neurobiology, Division of Biological Sciences, Cornell University, Ithaca, N.Y. (U.S.A.)

(Accepted November 16th, 1978)

The gaits of mammals can be subdivided into two main categories, symmetric and asymmetric. The former, including walk, trot and pace, show a strict alternation of the two limbs of one girdleZ. With the step cycle normalized t o 1, there is a phase difference of 0.5 between the two limbs. The asymmetric gaits form the remaining group, including the different types of gallop in which the phase difference between the limbs of one girdle may range from near 0 to approximately 0.4 (cf. Grillner4). As a consequence of the 0.5 phase shift in symmetric gaits, the limbs of a girdle perform their locomotor movements under the same conditions, landing, supporting, and flexing at the same relative points in the step cycle1,4. The situation necessarily differs in the asymmetric gaits. Despite the fact that clear asymmetries may be found in some records 2,7,10, most authors seem to use the simplifying assumption that the limbs are doing the same things (e.g. Miller and van der Mech67). However, little quantification has been made due to the difficulty of recording movements of both limbs simultaneously. The present paper investigates this problem. X-ray cinematography is used, observing the joint angles of both limbs simultaneously. Five male albino rats, 300-500 g, were trained to run in a modified exercise wheel (diameter 35 cm, width 12 cm) as described by Cohen and Gans 2. The wheel was self-driven with the animals permitted to run at their own pace. Once the rats were fully accustomed to the wheel, X-ray movies were taken and the films analyzed frame by frame (see legend, Fig. 1). To simplify the discussion, a new notation based on Philippson's terminology9 is used. He divided the step cycle into phases of flexion and extension of the limb. The unsupported flexion of the limb is denoted by F. The remainder of the step cycle is subdivided into an unsupported extension, Et and two support phases. Ez denotes the support phase during which the limb flexes under the weight of the body, and Ea, the phase during which the limb extends again. Proximal and distal joints are not necessarily synchronous in the initiation of the phases, thus the notation must specify Present Address for all correspondence:Department of PhysiologyIII, KarolinskaInstitutet,Liding6vagen 1, S-114 33 Stockholm,Sweden.

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Fig. 1. Right: drawing of the forelimb bones at the beginning of the stance (adapted from Jenkinse). The exercise wheel, used in the earlier study 2, was further modified for X-ray cinematography by replacing the two fiat faces with 1/8 inch plexiglass. Films were taken with a Siemens cinefluoroscopy unit at 35 or 45 kV and 220 mA. The image was intensified and filmed with an Auclair 16 mm camera at 50 or 100 frame/see. Frame by frame analysis was made by hand on a Vanguard Motion Analyzer. The angles measured arc indicated: a, the angle of the humerus with the ulna; b, the angle formed by the ulna with the horizontal; c, the angle of the scapular-humeraljoint; d, the angle formed by the humerus with the horizontal. The points taken as 0 °, 90 °, and 180° are marked for angles b and d. Left-hand graphs: asymmetric stride: changes of joint angles and change of angles formed by the bones with the horizontal. The upper traces are the angles of the shoulder and elbow joints. The bottom traces are the angles formed by the humerus and ulna with the horizontal at the corresponding times. Note the scales as indicated. Vertical lines indicate times of 'off' and 'on' for the stride. Beneath the graph are bars indicating the activity times of the muscles bridging the elbow. (EMG data are taken from Cohen and GansL) Abbreviations are: br, brachialis; bi lh, long head of the biceps; tri 1h, long head of the triceps; tri mh, medial head oftbe triceps; tri lh, lateral head of the triceps. Solid bars represent high levels of activity and dashed lines represent low levels of activity.

onset (O), p h a s e (F, El, E2, E3), right a n d left l i m b ( R , L ) a n d j o i n t s (e.g., elbow-e; shoulder-s). I n a s y m m e t r i c gaits the first a n d second limbs to strike the g r o u n d a r e specified as 1 a n d 2, respectively. T h e classical terms for the t w o limbs, trailing a n d leading, are n o t a p p r o p r i a t e here as they refer to spatial r a t h e r t h a n t e m p o r a l o r d e r o f c o n t a c t with the g r o u n d . I n the discussion the right l i m b will be a s s u m e d to strike the g r o u n d first. A c c o r d i n g l y : O F tte] a n d O F T M denote onset o f the flexion p h a s e for the e l b o w a n d s h o u l d e r o f the first limb. P a w ' o f f ' occurs s h o r t l y after this point. O E ~ ~l a n d O E Rsl d e n o t e onset o f the u n s u p p o r t e d extension. O E ~ "1 a n d O E ~ sl d e n o t e onset o f t h e yield flexion. F o r rats the onset o f E2 does n o t a l w a y s c o r r e s p o n d to p a w contact, as the long digits c a n t o u c h the g r o u n d before the l i m b begins to yield.

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Fig. 2. Change of elbow joint angles of both forelimbs during gallop. The simultaneous joint angles of the two limbs are superimposed with 'off' and 'on' indicated for each paw. Dashed lines and unfilled symbols are used for the first paw and solid lines and filledsymbols are used for the second paw. Onset of the phases of the step cycle are indicated using the notation defined in the text. There is 0.33 phase difference between the limbs in these strides. This graph and the preceding graphs are representative strides taken from two different animals. O E~e~ denotes onset of the stance extension. The intervals, denoted by their end-points, that correspond to Phillipson's step cycle are given for the elbow of the first limb. F: OFRoLOE~=I; ~' ,-,,~ael ,,~n,Rel nl~,Rel ¢31z'Rel. EoReI_OFRel. J ~ , l : L J £ , 1 - - L / E , 2 ; E2: v ~ . , 2 - - " ' ~ 2 , Es: A negative interval signifies that the second point precedes the first. Thus OE~ ~IOF Leg' < 0 is the interval from OF Le~ to OE2a*l. The angle values for the elbow of the two limbs differ at OF, PEt, and particularly OE2 (Fig. 2). The amplitude of the joint angle excursions during E1 are markedly different, being almost 50 % larger (27 °) in the first limb as compared to the second. Since the duration of Et is similar for both limbs, the angular velocity will be higher in the first limb. The amplitude of the joint angle excursion during E2 differs even more, due to a combination of the difference between OE2ael and O E ~ 2, and the similarity of OE~td and OE3LeE. In all asymmetric gaits OE2a~t begins much earlier in the step cycle than does OE Le2 (Fig. l graphs). Also, to prepare the limb for supporting the forequarters, the ulna of the first limb begins its descent well before ground contact. The second limb lands while the body is supported and continues extending until after paw contact. A further difference occurs at the end of Ea. At OF TM the humerus often rises all the way to a horizontal position or beyond, while the humerus of the second limb is rarely elevated beyond 30 ° (difference of 20 ° in Fig. 1 graphs). Thus, at the onset of the swing phase the configurations of the two limbs are different.

355 In symmetric gaits there are two equal periods of double support, OE2Ro--OFLe and OE~-OF Re. As animals 'break stride' there is an abrupt change in the value of these two intervals. They are only equal for the rare and extreme case of the full bound in which the two limbs strike the ground at precisely the same moment. The altered interlimb relationship can be seen in the simultaneous curves for the angles of both elbow joints (Fig. 2). The sole double support interval OE2~2-OFRel equals 15 ~o of the step cycles in the gallop illustrated. This interval is not at all similar to OE2Ret-OFLeL The latter interval is 73 ~ of the strides shown. It includes OE2Le2OF Re1 as well as two periods of single support, OE~I-OE2~2 and OFRel-OFLe2. The interval OE2R~I-OFLe2 < 0 is more closely related to the corresponding interval in symmetric gaits. The temporal order of the end points has been inverted by the change in interlimb coordination; in asymmetric gaits this interval marks the unsupported period. For all asymmetric gaits with OE2Le2-OFRel > 0 and OE~I-OFLe2 < 0, (Or > > 0), the following is seen. (1) OE~el occurs during an unsupported period. The first limb to land yields and provides single support until OE2Le2. Therefore, (2) OE L~2 occurs during a supported period. The second limb yields and helps provide double support until OF Rel. (3) OF ~el occurs during a supported period. The limb flexes and protracts leaving the second limb to provide single support until OF I'e2. Thus, (4) OF Le2 occurs during an unsupported period. The limb flexes and protracts while the forequarters are unsupported. The positions of the limbs relative to each other vary as a function of their phase coupling. In summary, the conditions under which the first and second limb strike the ground, provide support and flex are always mechanically quite different. The different mechanical demands are reflected in the movement asymmetries described above. At paw contact, the first limb must bear the full weight of the forequarters. The preparatory E1 of the first limb is effected by rapid rostrad movement of the humerus (Fig. 1 graphs), accompanied by an early onset of EMG activity in the double-jointed long head of the triceps 2. The timing of the other elbow muscles of both limbs is unchanged. Thus, there appears to be an asymmetry in the motor programs for the first and second limbs. This means that during asymmetric gaits, it should not be assumed that either the movements of the homologous limb pairs or their motor control are identical. The data presented here formed part of a doctoral dissertation submitted to the Division of Biological Sciences, Cornell University, under the direction of C. Gans and R. R. Capranica. The X-ray cin6 films were made in the laboratory of F. Jenkins, Jr.,MCZ, Harvard University, with the aid of E. Gordon. S. Grillner provided helpful comments on the manuscript.

1 Arshavsky,Y. I., Kots, Y. M., Orlovsky,G. N. Rodinov,I. M. and Shik, M. L., Investigationof the biomechaniesof running by the dog, Biophysics, 10 (1965) 737-746. 2 Cohen,A. H. and Gans, C., Muscleactivityin rat locomotion:Movementanalysisand electromyography of the flexorsand extensors of the elbow,J. Morph., 146 (1975) 177-195.

356 3 Gambaryan, P. P., HOw Mammals Run: Anatomical Adaptations, Halsted (Wiley), New York, 1974, (Transl. from the Russian edition, Nauka, Leningrad, 1972). 4 Grillner, S., Locomotion in vertebrates --central mechanisms and reflex interaction, PhysioL Rev., 55 (1975) 247-304. 5 Hildebrand, M., Analysis of the symmetrical gaits of tetrapods, Fol. Biotheor., 6 (1966) 9-22. 6 Jenkins, F. A,, Jr., The movement of the shoulder in claviculate and aclaviculate mammals, J. Morph., 144 (1973) 71-84. 7 Miller, S. and Van der Mech6, F. G. A., Movements of the forelimbs of the cat during stepping on a treadmill, Brain Research, 91 (1975) 255-269. 8 Philippson, M., L'autonomie et la centralisation dans te syst~me nerveaux des animaux, Tray. Lab. Physiol. lnst. Solvay Bruxelles, 7 (1905) 1-208. 9 Tokuriki, M., Electromyographic and joint-mechanical studies in quadrupedal locomotion. II1. Gallop, Jap. J. Vet. Sci., 35 (1974) 121-132.