Abstract. The pattern of locomotion following a partial movement re- straint was studied in five mongrel puppies. The locomotion of the ani- mals was ...
ACTA NEUROBIOL. EXP. 1989, 49: 39-46
Short communication
ALTERATION IN THE PATTERN OF LOCOMOTION FOLLOWING A PARTIAL MOVEMENT RESTRAINT IN PUPPIES Janusz W. BEASZCZYK and Czeslawa DOBRZECKA Department of Neurophysiology, Nencki Institute of Experimental Biology 3 Pasteur Str., 02-093 Warsaw, Poland
KCU ~uords:locomotion, movement restraint, gait alteration
Abstract. The pattern of locomotion following a partial movement restraint was studied in five mongrel puppies. The locomotion of the animals was characterized by enforced pacing during the restraint peri-od and exhibited significant, time dependent gait alterations after removal of the restraint. These changes involved gradual recovery to normal trotting. The time course and the degree of recovery in the animals were dependent on the period of movement restraint. Puppy that was forced to practice pacing for only two months switched almost instantaneously to the normal trotting, whereas in those dogs with a longer selective movement restraint, a significant long lasting incidence of pacing was observed. The study describes an animal model which can be useful a s tool in future studies of the plasticity of motor system and its basic mech:~nismsin various physiological conditions. Most animals use locomotion strategies that optimize (usually minimize) energy consumption (5). Probably for this reason different species have developed the same or similar locomotor patterns of limb coordination. There are many different classifications of quadrupedal gaits. One of them, based on the phase relationships between limb movements, distinguished symmetrical and nonsymmetrical patterns of locomotion (9, 10-12). The symmetrical gaits, mainly represented by walk, trot and pace, are characterized by reciprocity of fore- as well as hind-limb
movements (the intragirdle phase difference is equal to 0.5) whereas nonsymmetric gaits consisting of different kind of gallops, are described by intragirdle phase shifts less than 0.5. All symmetrical gaits have their own characteristic phase difference between particular limb movements. These phase differences do not depend on the velocity of locomotion (2). Depending on phase relation between fore and hindlimbs one can distinguish symmetrical gaits with diagonal (trot) and lateral (pace) patterns of coordination. The diagonal support is widely accepted as the basic element of locomotion in quadrupeds (for references see 6). Even gaits such as the walk or the transverse gallop also involve diagonal elements In four llmb cycle and can therefore be treated as functional modifications of the trot (2). However, it has been observed that in some dogs, horses, cats running on the treadmill (13), as well as in camels and glraffes etc., pacing is commonly used instead of trotting in the middle range of locomotion velocities. Pacing appears to dominate in animals whose limbs are relatively long with respect to their interlimb-girdle spacing. This led us to propose that a change from a diagonal to unilateral pattern of coordination might be induced by certain agents acting on the motor system. We expected that especially during early stage of gait development the motor system should be the most flexible for any gait modification. It is known that without any previous locomotor experience, animals can develop unique locomotor pattern. Some mammals can walk soon after birth (10). Other mammals, including dogs and cats are immature when born and only begin to walk when the maturation of the nervous and muscular systems reaches a certain level (for references see 7, 8). It is assumed that gait development in animals and humans is related to this genetically controlled maturation process rather than learning (9). To determine the role of the learning process in gait development and to verify plasticity of the central pattern generator (CPG) we decided to study changes in the limb coordination following selective movement restraint in puppies. Experiments were performed on 8 mongrel puppies of either sex of two different litters. Three puppies served as a control group. The unilateral limbs of the rest five two-week old puppies were tled together with a soft cotton belt in such a way that they were able to move using the unilateral pattern of limb coordination (pacing) only (Fig. 1). The length of the cotton belt was equal to their intergirdle distance and was adjusted as the animals grew. During the restraining period the puppies were allowed to walk and run in their cages. They were also trained to move along the experimental platform and their footfall pattern was monitored using special purpose contact electrodes. The ele-
ctrodes were constructed from a tiny soft copper braid placed on the third digit of each paw (the method is described in details in reference 1).
Fig. 1. One of the experimental animals (dog A) shown wearing the movement restraint.
The experimental pathway was 8 m long and 1 m wide and co'nsisted of soft wire netting. The ends of the platform were connected to a low voltage dc power supply so that a linearly increasing voltage, from 0 to 70 mV was obtained along the pathway. This allowed us to record 2-dimension gait diagrams (1-4). The diagram (Fig. 2) includes information about temporal (swing-stance durations) and spatial stride length) movement parameters recorded for all four limbs simultaneously. In 2-D gait .diagrams the low level signal (base line) corresponds to the swing phase. Contact of a limb with a pathway produced a square pulse where height corresponds to position of that limb on the platform and where its width represents stance phase duration. A difference in amplitude of two successive stance signals determinates a stride length. Each of the 5 puppies was subjected to movement restraint periods of from 2 to 6 months respectively (Table I). After restraint cessation gait diagrams of untied dogs were observed and recorded twice a week for a first six weeks and once a week for the next two months. The results of five post-restraint weeks for all animals are shown in Table I. During each experiment subjects were running along the experimental pathway and their 2-D gait diagrams were recorded on the ink recor-
Fig. 2. Two-dimensional gait diagrams for one of the experimental animals (dog A) showing the usual trot pattern, characterized by diagonal limbs synchronization (A) and the acquired pace pattern with a typical unilateral limb; synchronization (B). T, labels the time marker (seconds). R F , right forelimb; LF, left forelimb; RH, right hindlimb, and LH, left hindlimb. The traces show particular foot contact recordings. The base lane sectors correspond to the swing phases, whereas the amplitude and length of high level signals indicate position of a foot on the experimental pathway and stance phase duration, respectively.
der. The number of runs was not strongly forced by experimenters but
we usually tried. to record a similar number for all of the animals. The diagrams recorded were classified as diagonal or lateral on the bzsis of the phase difference between unilateral limbs (phase differences 0 and
TABLEI Results from first five succeessive, post-restraint weeks showing number of strides with unilateral (pacing) and diagonal (trotting) limb coordinations in all experimental puppies. Gallop not included -Restraint period Experimental Number of strides I'UPPY (months) session pace trot
5
D
5
412 423 273 256 212
760 460 647 504 486
1 2 3 4 5
88 269 73 73 41
55 186 194 501 408
1 2 3 4 5
0 0 0 0
480 460 420
1 2 3 4
-
- -
--
-
E
6
-
-
--
--
Control 1
-
-
-
Control TI
-
--
--
- - - -
0
- -
-
- -
--
Control 111
--
-
0
- -
0
-
- -
- -
-
-
- -
-
-
1 2 3 4 5
0 0 0 0
1 2 3 4 5
0 0 0 0 0
--
-
384 400 288 108 480 380 560 280 200
--
-
-
- .
0.5, respectively, for pacing and trotting). From all diagrams recorded, a number of strides with particular gait pattern were calculated. The percentage of strides of pace with respect to total number of strides during five successive post-restraint weeks are shown in Fig. 3.
POST-RESTRAINT
RECOVERY
POST-RESTRAINT SESSION
Fig. 3. Bar graph showing percentage of lateral gait for experimental animals (A-E) and the control group for each week after discontinuation of movement restraint.
All of the restrained subjects habituated very quickly to the restraint. All puppies studied started to walk on about the fourth week of life. However, the selective movement restraint retarded the very beginning of their movement development in compsrison with the control group. After a few days restrained animals started to pace and the difference in mobility of these two groups disappeared. Pacing occurred in a wide velo'city range for the restrained group animals while the puppies from the control group used only the trot and transverse gallop in the same range of spee,d. Pacing during the post-restraint period was observed in all animals and this pattern was recorded during the entire period of observation (over 6 months). However, the animal with two month restraint period, during the first post-restraint experiment perfor-
med a couple of runs with pacing and then switched to trot. But even 6 months after restraint was discontinued, we observed episodes of pacing from time to time. Also, it preferred a rotatory gallop to a transverse gallop which is more common for mongrel dogs (2). In the remaining restrained puppies the number of runs with lateral limb coordination depended on the restraint period. Longer restrained puppies had a greater amount of strides with pace coordination (up to 61.5"/d in animal E after six months of movement restraint, compared to anima'l A at 7.6OIo). In the majority of puppies the percentage of paced stride,s in relation to total number of strides (except galloping) during each experiment decreased with time of observation (Fig. 3), but even after six weeks of recovery we still observed from 1.2 to 30.4"/0 of the total number of strides weire paced. The results suggest the existence of correlation between restraint period and both number of pacing strides and length of post-restraint recovery. Movement restraint lasting longer than three months postnatally .seems to be very important for creating entirely new interlimb coordination. The importance of this period in movement development in puppies has been stressed by several authors (e.g. 7, 8). During this period of extensive development the motor control system seems to be m.ore eslsily modified in structure and/or function. The results presented here support the idea that the main structure and function of central pattern generator (CPG) is genetically determined. Even animals having no chance to practice diagonal gaits because of movement restraint can develop this pattern of lo~o~motioin. They can switch from pacing to trotting almost in the first trials of recovery from restraint and diagonal limb coordination soon becomes as perfect a,s in the animals from control group. The restrained animals used either diagonal or lateral gaits. Recovery from restraint points out preference for trotting as a much more efficient gait (3). However, long lasting movement restraint causes the development of a new pattern of locomo~tion that was never observed in the control group animals. So, there is a possibility that the diagonal structure of CPG can be functionally modified. This suggests that either all diagonal and lateral patterns are encoded in the CPG structure, or there is additional system controlling limb phase relationships which under certain conditions (e.f., strong peripheral input) allows switching from trotting to pacing, as observed in the cats running on the treadmill (12). In these preliminary experiments we wished to determine whether it was possible to persistently reorganize the CPG anatomical or functional structure and whether there is any critical point in an animal's movement development which allows us to do this. Although our results
confirm the possibility of gait repertoire modification, the question remains whether these changes are the result of CPG circuitry modifications andlor supraspinal learning processes. 1. AFELT, Z., BEASZCZYK, J. W. and DOBRZECKA, C. 1983. Stepping frequency and stride length in animal locomotion: a new method of investigation. Acta Neurobiol. Exp. 43: 227-234. 2. AFELT, Z., BEASZCZYK, J. W. and DOBRZECKA, C., 1983. Speed control in animal locomotion: transitions between symmetrical and nonsymmetrical gaits in the dog. Acta Neurobiol. Exp. 43: 235-250. 3. BEASZCZYK, J. W. and DOBRZECKA, C. 1985. Control of locomotion velocity in tetrapods. Acta Physiol. Bohemoslov. 34 (Suppl.): 9-13. 4. BEASZCZYK, J. W. and C. DOBRZECKA. 1986. Two-dimensional gait diagrams applied t o t h e study of normal and pathological gaits. Satelite Symposium to t h e XXX Inter. Cong. of Physiol. Sciences. "Novel Approaches to t h e Study of Motor Systems". Banff, Canada 10-13 July, 1986, p. 6-7. 5. CAVAGNA, G., NORMAN, A., HEGLUND, C. and TAYLOR, C. R., 1977. Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. J. Physiol. 233 (5): R243-R261. 6. GAHERY, Y., JOFFE, M., MASSION, J. and POLIT, A. 1980. The postural support of movement i n cat and dog. Acta Neurobiol. Exp. 40: 747-756. 7. GOLDBERGER, M. E. 1986. Segmental and suprasegmental contributions to development and recovery of motor function in kittens. In S. Grillner, P. S. G. Stein, D. G. Stuart, H. Forssberg, and R. M. Herman (ed.), Neurobiology of vertebrate locomotion. Vol. 45. Wenner-Gren Center International Symposium Series, Macmillan. p. 455-483. 8. GORSKA, T. and CZARKOWSKA, J . 1973. Motor effects of stimulation of t h e cerebral cortex in t h e dog. A n ontogenetic study. In A. A. Gydikov, N. T. Tankov, and D. S. Kosarov (ed.), Motor Control. Plenum Press, New York, p. 147-166. 9. GRILLNER, S. 1984. Control of locomotion in bipeds, tetrapods, and fish. In J. M. Brookhart and V. B. Mountcastle (ed.), Handbook of Physiology. The nervous system. Vol 11. American Physiol. Soc. Bethesda, Maryland, p. 1179-1236. 10. HOWELL, E. B. 1944. Speed in Animals. Chicago, Hafner, p. 195-270. 11. MUYBRIDGE, E. 1957. Animals in motion. Dover Publications Inc., New York, 183 p. 12. WETZEL, M., ATWATER, A,, WAIT, J. and STUART, D. 1975. Neural implication of different profiles between treadmill and overground locomotion timing in cats. J. Neurophysiol. 38: 492-501. 13. WETZEL. M. C. and STUART, D. G. 1976. Ensemble characteristics of cat locomotion and its neural control. In G. A. Kerkut and J. Phillis (ed.), Progress i n Neurobiology. Vol 7, Pergamon Press, Oxford, p. 1-99. Accepted 10 August 1988
