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Brain Research, 100 (1975) 17~174 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

Motor performance following unilateral pyramidal tract lesions in the hamster

KATHERINE KAL1L* AND GERALD E. SCHNEIDER Department of Psychology, Massachusetts Institute of Technology, Cambridge, Mass. 02139 (U.S.A.)

(Accepted August 26th, 1975)

A number of studies have shown that the pyramidal tract plays an important role in the fine motor control of the forelimb in monkeys2,~,9,13. Following transection of the pyramids, for example, movements of individual digits are permanently impaired 9. Less is known about the function of the pyramidal tract in non-primate species. However, several studies have demonstrated that in the rat 1,4 and the brushtailed possum 6, the pyramidal tract is also involved in the execution of discrete movements of the limbs. In order to provide further information about the role of the pyramidal tract in the motor behavior of rodents, we made unilateral lesions of the pyramidal tract in adult golden hamsters (Mesocricetus auratus) and studied their effects upon motor performance. Prior to making the lesions, we observed the normal motor behavior of the hamsters in grooming, climbing, walking and feeding. We tested the hamster's ability to grasp and manipulate small objects by presenting them with unshelled sunflower seeds. The descriptions of the animals' motor behavior are based on observations made daily for the first 3 postoperative weeks and then at weekly intervals for periods up to 14 months. In addition, both pre- and postoperative motor behavior was recorded and analyzed on 800 ft. of 16 mm film and several hours of videotape. Pyramidal tract lesions were made according to the method described by Barron 1. The animals were anesthetized with chloral hydrate and sodium pentobarbital (Equi-Thesin), and the medullary pyramids exposed by a ventral approach through the basi-occipital bone. With a fine knife, the pyramid was cut on one side just rostral to the pyramidal decussation. Ten out of 14 animals survived this procedure; of these 5 survived for over 10 months. The motor behavior of the 10 animals was observed for postoperative times ranging from 2 weeks to 14 months. They were then re-anesthetized and perfused through the heart. The brains were removed from the skull, photographed, immersed in 30 ~ sucrose-formalin and cut at 30/zm in the transverse or parasagittal plane on a freezing microtome. Closely spaced series of sections in the region of the lesion were stained with cresylecht violet, method ! of Fink and Helmet, and the Loyez method. The anatomical results of these experiments have been published elsewhere 5. * Present address: Department of Anatomy, University of Wisconsin, Madison, Wisc. 53706, U.S.A.

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Fig. 1. Photomicrographs of Nissl-stained coronal sections through the medulla of two hamster brains to illustrate typical unilateral transections of the pyramidal tract. In both cases the normal pyramidal tract (PT) is on the right and the lesion (arrow) is on the left.

T h e lesions were s o m e w h a t variable in their extent. I n all cases, however, there was virtually c o m p l e t e t r a n s e c t i o n o f the p y r a m i d a l t r a c t on one side (see Fig. 1). Occasionally, there was slight d a m a g e to the medial fibers o f the c o n t r a l a t e r a l p y r a mid, a n d there was usually slight to m o d e r a t e involvement o f the ipsilateral medial

172 lemniscus. This damage was assessed by anterograde degeneration appearing in the medial lemniscus as well as observations made on Nissl-stained sections. The quality of the motor deficits was similar in all animals, though some were more severely affected than others. Following recovery from anesthesia, the animals all exhibited weakness of the limbs contralateral to the lesion. They could no longer climb out of their cages by grasping the edge of the cage with the affected forepaw. In walking on a wire mesh, the fore- and hindlimbs opposite the lesion often slipped through the holes. On a solid surface, the affected forepaw was frequently bent backwards so that the animal walked on the back of the wrist. This limb was displaced toward the midline and tended to cross under the normal forelimb. Some animals hyperflexed the forelimb and hyperextended the hindlimb opposite the lesion. Except for one case in which there was persistent hyperextension of the hindlimb, most of the deficits in locomotion and climbing passed away within several weeks. Significantly the complex stereotyped grooming behavior was by and large unaffected by the lesion. In grooming, the hamster rubs the forepaws together, licks them, and rubs them over the face and ears. The belly, flanks, and hindlegs are groomed with the mouth and by rapid flexion of the digits in rubbing and digging motions. The normal hamster has a remarkable ability to make precise manipulations with its digits. We elicited this behavior by feeding the animals large unshelled sunflower seeds. In tearing the shells off with its teeth, the hamster continually turns and manipulates the seeds using fine digital movements. While the hamster cannot flex a single digit, the digits do appear to flex sequentially as a continuous motion. These movements were repeatedly observed with slow motion videotapes. In handling seeds, grasping food, or grooming, the normal animal always uses both forelimbs. Thus, after the lesions, the abilities of the affected limb could be compared with the normal side to evaluate the motor deficits. The cl~,aracteristic motor disability following unilateral transection of the pyramidal tract was a permanent impairment in manipulatory movements of the contralateral forepaw. For several days after surgery the animals were unable to grasp food with this limb, and during the early stages of recovery food often slipped out of this paw. For several weeks the animals did not attempt to manipulate food, and when they tried to do so the seeds and pieces of food fell to the floor of the cage. The hamsters tended to adopt a characteristic feeding posture in which the normal forelimb crossed over the midline to grasp food and the affected limb merely served as a passive support for the seeds (see Fig. 2). Even after a year, the affected forepaw never regained the precise manipulatory capabilities observed prior to the lesion. The digits of this limb clasped and unclasped as a unit and were often cupped tightly together instead of flexing in their normal rapid sequence. The handling of sunflower seeds often involved whole arm scooping or hooking motions and the use of the wrist rather than the palm or digits of the affected forelimb. Although the animals could use this paw in grasping, the seeds gradually slid onto the wrist and the animal had to continually regrasp them. In order to control for the possibility that the motor deficits described above resulted from trauma to the spinal cord during surgery, unilateral lesions at upper cervical levels were made in the spinal cords of 5 animals. The lateral and ventral

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Fig. 2. Drawing made from 16 mm film of a hamster with a lesion of the left pyramidal tract. Note that the digits of the animal's normal left forepaw are spread out and slightly flexed to manipulate the sunflower seed, whereas the digits of the forepaw opposite the lesion are cupped together and are passively supporting the seed.

funiculi were damaged in all cases but the dorsal columns and the underlying pyramidal tract were completely spared. These animals, unlike those with pyramidal tract lesions, had no difficulty in grasping and manipulating sunflower seeds with the forepaw ipsilateral to the spinal cord lesion. However, they did display an abnormality in their grooming behavior. While the animals could rub the forepaws together, the limb ipsilateral to the lesion remained extended in front o f the animal and was not flexed to rub the face and ears. Moreover, in trying to unpouch sunflower seeds they repeatedly failed to touch the cheek pouch with the affected forepaw though they made vigorous movements of the shoulder. Even after several months and some recovery o f function, smooth normal grooming motions never returned to this limb. Though the variety in the extent of the lesions makes it difficult to relate this motor defect to a specific pathway in the spinal cord, it might be suggested that difficulties in grooming resulted from a failure to flex the muscles of the forelimb, a function associated with the rubrospinal tract 11. Nevertheless, the control experiments clearly demonstrate that the loss in digital ability observed after pyramidal tract lesions did not result from damage to other pathways in the spinal cord. These results show that after unilateral interruption of the pyramidal tract, the hamster retains or is able to recover a wide range of motor behavior. However, the precise manipulatory ability of the contralateral forepaw is permanently impaired. Previous reports have shown that pyramidal tract lesions result in impairment in the

174 accurate p l a c e m e n t o f the limbs in cats 1° a n d o p o s s u m s 6, and in the digital ability in monkeys9, la a n d rats 1,4. W h e r e a s previous a u t h o r s l , 4 have e m p h a s i z e d a deficit in the rat's ability to grasp food with the forelimb after p y r a m i d a l tract section, we have d e m o n s t r a t e d a m o r e specific deficit in the ability o f the h a m s t e r to execute precise m a n i p u l a t i o n s with its digits. We have also observed t h a t in hamsters, lesions o f the p y r a m i d a l tract d o n o t seem to p e r m a n e n t l y affect s t e r e o t y p e d behaviors such as l o c o m o t i o n o r grooming. The p y r a m i d a l tract m a y p l a y an i m p o r t a n t role in m a n i p u l a t o r y or e x p l o r a t o r y behaviors which are heavily d e p e n d e n t u p o n sensory f e e d b a c k for their precise execution. Recently it was d e m o n s t r a t e d in the m o n k e y t h a t the m o t o r cortical efferent zones p r o j e c t i n g to specific muscles o f the distal forelimb receive p e r i p h e r a l afferent inputs from the skin, joints, a n d muscles o f t h a t same forelimb r e g i o n l L A similar neural substrate m a y underlie the precise m a n i p u l a t o r y behaviors o f the rodent, since these abilities are p e r m a n e n t l y i m p a i r e d when the p y r a m i dal tract is cut. Thus, despite the evidence t h a t the r o d e n t a m a y lack the direct corticom o t o n e u r o n a l connections d e m o n s t r a t e d in p r i m a t e s 8, a c o m p a r a b l e m o t o r deficit is f o u n d in both orders o f animals when the p y r a m i d a l t r a c t is interrupted. We t h a n k Miss Lucy T a y l o r for the d r a w i n g o f the hamster. S u p p o r t e d by U S P H S G r a n t EY-00126, N S F Training G r a n t GZ-2385 and a grant from the Alfred P. Sloan F o u n d a t i o n .

1 BARRON, D. H., The results of unilateral pyramidal section in the rat, J. comp. Neurol., 60 (1934)

45-55. 2 BECK, C. H., AND Cr~AM~ERS,W. W., Speed, accuracy and strength of forelimb movement after unilateral pyramidotomy in rhesus monkeys, J. cornp, physiol. Psychiol., 70 (1970) 1-22. 3 BROWN,L. T., Projections and termination of the corticospinal trac~ in rodents, Exp. Brain Res., 13 (1971) 432~[50. 4 CASTRO,A. J., Motor performance in rats. The effects of pyramidal tract section, Brain Research, 44 (1972) 313-323. 5 HEPP-REYMOND,M. C., AND WIESENDANGER,M., Unilateral pyramidotomy in monkeys: effect on force and speed of a conditioned precision grip, Brain Research, 36 (1972) I I 7-131. 6 HORE,J., PHILLIPS, C. G., AND PORTER, R., The effects ofpyramidotomy on motor performance in the brush-tailed possum, Brain Research, 49 (1973) 181-184. 7 KALIL, K., AND SCHNEIDER,G. E., Retrograde cortical and axonal changes following lesions of the pyramidal tract, Brain Research, 89 (1975) 15-29. 8 KUYPERS,H. G. J. M., Central cortical projections to motor and somato-sensory cell groups. An experimental study in the rhesus monkey, Brain, 83 (1960) 161-184. 9 LAWRENCE,D. G., AND KUYPERS,n. G. J. M., The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain, 91 (1968) 1-14. 10 LIDDELL,E. G. T., AND PHILLIPS,C. G., Pyramidal section in the cat, Brain, 67 (1944) 1-9. 11 MASSION,J., The mammalian red nucleus, Physiol. Rev., 47 (1967) 383~J,36. 12 ROSEN,I., AND ASANUMA,H., Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-output relations, Exp. Brain Res., 14 (1972) 257-273. 13 TOWER,S., Pyramid lesion in the monkey, Brain, 63 (1940) 36-90.

Motor performance following unilateral pyramidal tract lesions in the hamster.

170 Brain Research, 100 (1975) 17~174 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands Motor performance following u...
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