Brain Research, 89 (1975) 15-27


© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands




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

(Accepted December 24th, 1974)


Following lesions of the pyramidal tract in hamsters, retrograde changes were studied in the sensorimotor cortex and in the pyramidal tract axons proximal to the lesion, at survival times ranging from 2 weeks to 14 months. Severe cell shrinkage occurred in layer 5 pyramidal neurons as early as 2 weeks, but there was no cell loss among these neurons even with long survival times. Use of the F i n k - H e i m e r method for degenerating axons revealed that the pyramidal tract proximal to the lesion had undergone a retrograde axon degeneration which, in some respects, resembled anterograde degeneration. The retrograde axon degeneration began at the lesion site and advanced slowly rostralwards with time involving increasingly greater numbers of fibers. However, even at the longest survival times the degeneration fell offmarkedly at pontine levels. The results indicate that this process represents a true retrograde fiber degeneration (as opposed to an indirect Wallerian degeneration) which appears to reach a point of equilibrium such that a partially shrunken pyramidal cell is maintaining a partially degenerated axon.


In the course of a study of motor abilities in hamsters following lesions of the pyramidal tract, it was noted that the pyramidal tract central to the lesion had undergone some unexpected anatomical changes 16. Moreover, some of the cells of origin of the pyramidal tract in the cerebral cortex were also structurally modified, even when the survival times were relatively short. Since retrograde fiber changes have not often been described with modern silver techniques, and since controversy exists concerning * Present address: Department of Anatomy, University of Wisconsin, Madison, Wisc. 53706, U.S.A.

16 the fate of both the proximal axon segment and the cell bodies of origin after section ol the pyramidal tract, it seemed worthwhile to report these anatomical results. MATERIALS AND METHODS

Ten adult Syrian hamsters (Mesocricetus auratus) were used in this study. The animals were anesthetized with chloral hydrate and sodium pentobarbital (EquiThesin, 0.35 ml/100 g) and the medullary pyramids exposed, according to the method described by Barron 4, with a ventral approach through the basi-occipital bone. With a fine surgical knife, the pyramidal tract was cut unilaterally just rostral to the pyramidal decussation. Care was taken to minimize damage to deeper lying structures, particularly the medial lemniscus. The animals were allowed to survive for periods ranging from 2 weeks to 14 months. One animal was sacrificed at each of the following survival times: 2 weeks, 4 weeks, 2 months, 4 months, 10 months, 12 months (2 animals), 13 months, and 14 months (2 animals). Following an overdose of anesthetic, the animals were perfused through the heart with 10 ~ formol-saline. The brains were removed from the skull, further hardened in the fixative, photographed, immersed in 30 sucrose-formalin for several days, and then cut at 30 #m on a freezing microtome. Most of the brains were cut in the transverse plane, but in several cases the brain stem and upper cervical spinal cord were cut parasagittally, and the more rostral block was cut transversely. One in every 3 or 6 sections of the brain stem and cord was stained with method I of Fink and Heimer 11 for degenerating axons and an adjacent series was stained with cresylecht violet. Every third section through the forebrain was also stained with cresylecht violet. RESULTS

The cerebral cortex Two weeks following section of the pyramidal tract there was a marked alteration o f the large pyramidal neurons in layer 5 of the sensorimotor cortex ipsilateral to the lesion. At first examination it appeared that all of the large pyramidal cells in this layer had disappeared. However, a close inspection of individual pyramidal cells in this layer as well as counts of these neurons on both sides of the brain (see Table 1) revealed that there was no significant cell loss; rather, there was substantial shrinkage of most of the large pyramidal cet Is in layer 5. The cell shrinkage appeared to be very great by 2 weeks (Fig. 1) and the brains of animals that had survived up to one year revealed no significant further changes either of degeneration or recovery by the pyramidal cells. Particularly striking were changes in the cortical cells of an animal that survived for 2 months (Fig. 2). On the normal side, layer 5 pyramidal cells are large neurons easily identifiable by their shape and prominent apical dendrite, which is often stained over a considerable distance. On the side of the lesion the affected pyramidal cells could be recognized by their prominent apical dendrites and triangular shape accentuated by a shrinkage that sometimes amounted to 50 ~ in area. Moreover, many of the shrunken cells stained more deeply than their normal counterparts.









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hamster surviving 2 weeks after a left sided pyramidal tract lesion. Since the lesion was made above the decussation, retrograde changes are observed ipsi[ateral to the lesion. Note band of large pyramidal cells in layer 5 in cortex on the right (contralateral to the lesion) and their apparent absence in cortex on the left (ipsilateral to the lesion).

The p y r a m i d a l traet

In the cervical spinal cord distal to the transection, the pyramidal tract exhibited the typical appearance of Wallerian degeneration. As stained with the Fink-Heimer H method for degenerating axons, the pyramidal fibers below the lesion appeared as rows of somewhat coarse bead-like silver fragments• This degeneration, though diminishing slightly and growing more granular with time, persisted for as long as a year after the lesion. Proximal to the lesion, the pyramidal tract contained varying numbers of silver impregnated axons, which in many respects resembled axons undergoing Wallerian degeneration. Since the numbers, distribution, and appearance of axons undergoing this retrograde degeneration depended on the survival time and the plane of section, results will be described for representative survival times• A t 2 and 4 w e e k s survival time (parasagittal plane) there was a region of intense glial proliferation extending about 0.75 mm rostral to the lesion which was made at the caudal level of the inferior olive. In this region the axons were severely disrupted and




Fig. 2. Photomicrographs of Nissl-stained layer 5 pyramidal cells in sensorimotor cortex (coronal section) of a hamster surviving for 2 months after left sided pyramidal tract lesion. A and B ~re taken from opposite sides of the same section. Lesion (illustrated in Fig. 3) is rostral to the dccussation. A: illustrates shrunken pyramidal cells (see arrow) in cortex ipsilateral to the lesion. Compz~red with normal cells (B) shrinkage is at least 50 %. Note their well defined apical dendrites and obvious pyramidal shape. Layer 4 granule ceils visible at top of photomicrograph. B: illustrates nom~al pyramidal cells (see arrow) contralateral to the lesion.

there were numerous silver fragments in various orientations. In the next 1.5 mm segment, extending almost to the caudal boundary of the trapezoid body, the fibers resumed their normal orientation, but scattered sparsely among the normal axons were some which were either beaded or fragmented. Only a few axons undergoing this retrograde degeneration could be identified at the level of the trapezoid body. At 4 weeks survival time there was a moderate increase in the number of beaded or fragmented axons over those that could be observed after 2 weeks. A t 2 months survival time (transverse plane) a marked axonal reaction was observed which extended from the lesion site, at the mid inferior olivary level, to the caudal region o f the trapezoid body. Cut in the transverse plane, the axons o n the intact side appeared as smooth, amber colored, round or ellipsoid profiles. By contrast, the axons above the lesion stained black and were smaller than the normal ones. Moreover, for several mm above the lesion the affected pyramid was shrunken in area by about 15 and punctuated with irregular granular silver particles (cf. Fig. 4). A t 4 months (transverse plane) greater numbers of axons became darkly impregnated with silver and there was an increased proliferation of granular silver debris in the shrunken pyramidal tract above the lesion. The number of affected axons at the

19 TABLE I COUNTS OF PYRAMIDALCELLS IN LAYER 5 OF SENSORIMOTORCORTEX CONTRALATERALAND IPS1LATERALTO LESIONS OF THE PYRAMIDAL TRACT, AFTER VARIOUS SURVIVAL TIMES Cell c o u n t s represent n u m b e r o f p y r a m i d a l cells (on a single coronal section) in an area of sensorim o t o r cortex that filled 3 adjacent fields of the microscope using a • 25 objective. C o u n t s were m a d e in exactly c o r r e s p o n d i n g regions of opposite h e m i s p h e r e s o f the s a m e section. S h r u n k e n p y r a m i d a l cells on the side of the lesion were identified as p y r a m i d a l by their s h a p e a n d the presence of an apical dendrite.

Brain No.

Pyr Pyr Pyr Pyr Pyr

8 9 7 1 2

Survival time

2 weeks 1 month 2 months 4months 12months

Numbers oJ layer 5 pyramidal cells Normal cortex (contralateral to lesion)

Abnormal cortex (ipsilateral to lesion)

333 439 345 322 417

331 444 395 350 462

level of the trapezoid body had markedly increased over those seen at 2 months. However, retrogradely degenerating axons were still sparse in the pons. At 13 months survival time, in a case cut in the parasagittal plane, axons proximal to the lesion bore an especially strong resemblance to axons undergoing Wallerian degeneration. Between the lesion, just caudal to the inferior olive, and the pons, a distance of about 5 mm, the amount of silver degeneration products was massive (Fig. 5). Rows of irregularly shaped silver droplets were interspersed with round granular fragments of silver-stained material. Many of the pyramidal tract fibers had a continuously beaded or varicosed appearance which differed from typical ~lnterograde degeneration primarily in that the beads were much smaller. Whereas the anterograde degeneration had the appearance of large beads linked together by a much finer filament, the axons undergoing retrograde degeneration often took the form of small beads only slightly larger than the processes which joined them together. This result suggests that perhaps the retrograde axonal degeneration was accompanied or preceded by atrophy of the nerve fiber. Moreover, the granular, wispy quality of the silver product associated with the proximal axon segment is characteristic of Wallerian degeneration of long-standing. There was a dramatic decrease in the number of degenerating axons at caudal pontine levels, though a significant number could still be observed throughout the pons. At 10, 12, and 14 months survival (transverse plane), the retrograde axonal degeneration was very heavy at levels up to the ports and the shrinkage of the pyramid was about 30 ~ . However, there were many fewer degenerating axons in the ports and only a small number could be followed into the cerebral peduncle. None could be reliably identified in the internal capsule at any survival time. The temporal progres-


Fig. 3. Ventral view o f a hamster brain to show typical location and extent o f a pyramidal lesion (arrow) made just rostral to the decussation. Scale is 2 ram.

sion of the retrograde axon degeneration over a maximal distance of 6-7 m m rostral to the lesion is summarized in Fig. 6. DISCUSSION

General interpretation These experiments show that following transection of the pyramidal tract there is a relatively rapid shrinkage of the large pyramidal cells o f layer 5 in the sensorimotor cortex. Since 2 weeks was the shortest survival time used, it is possible that the retrograde atrophy of cortical neurons occurs even earlier. It is also possible that the smaller pyramidal cells in layers 3 and 5 or even perhaps other cell types may u n d e r g o a similar atrophy, but this was not obvious in the material, and measurements of these cells were not made. It seems unlikely that a major cell loss occurred in the cortex, since the number o f shrunken pyramidal neurons remaining on the side of the lesion was comparable to the number of large pyramidal cells in layer 5 of the intact side (see Table 1).


Fig. 4. Photomicrographs of normal (A) and degenerating (B) pyramidal tract fibers 3 mm rostral to the lesion. Fink-Heimer stain, coronal section. Animal survived for 12 months after the lesion. Appearance of degenerating fibers is typical of survival times from 2 to 14 months, though their numbers and distribution vary with time. A : note pale roundish normal axons (arrow). B: note deeper staining shrunken degenerating axons (arrow) and granular silver particles.

The changes occurring in the pyramidal axons proximal to the lesion constitute a true retrograde axon degeneration in which beaded or fragmented argyrophilia is present. It is clear, however, that the retrograde and anterograde axonal degenerative processes have a different time course since the anterograde degeneration in the pyramidal tract is well advanced in less than 1 week, whereas the retrograde degeneration progresses slowly over several months. The smaller diameter and finer beading observed in axons undergoing retrograde degeneration suggest that this process may be preceded by an atrophy of the nerve fiber. The results suggest that atrophy of cortical neurons takes place before there is a substantial reaction in the proximal axons, since at 2 weeks survival there is massive shrinkage of the cortical neurons whereas retrograde axon degeneration as observed with the light microscope, has progressed only a few millimeters proximal to the lesion and involves relatively few axons. The retrograde axon degeneration advanced slowly rostralwards towards the cell body of origin, but even with survival times of one year there was a marked fall off of such degeneration at pontine levels. The cerebral cortex

Previous studies of retrograde cortical changes after pyramidal tract lesions are


Fig. 5. Photomicrograph of retrogradely degenerating axons about 3 mm proximal to a pyramidal tract lesion. Fink Heimer stain, parasagittal plane. Animal survived for 13 months. Note beaded and fragmented axons. Granular silver particles shown in inset were photographed frown an adjacent region of the section at the same magnification. c o n t r a d i c t o r y on several points. In their classic study, H o l m e s a n d M a y 15 observed that r e t r o g r a d e changes in the cortex consisted o f c h r o m a t o l y s i s , shrinkage, a n d eventual d i s a p p e a r a n c e o f a large p r o p o r t i o n o f the g i a n t Betz cells in the m o t o r cortex. Their estimates o f p y r a m i d a l cell loss r a n g e d f r o m 75 ~ in a d o g t h a t survived 23 days to over 9 0 ~ in a m o n k e y that survived for 57 days. However, they c o n c l u d e d that



Les 2 - 4 W 2



Fig. 6. Schematic representation of parasagittal view of a hamster brain, to show rostralward temporal progression of retrograde axonal degeneration in the pyramidal tract. At bottom, lesion is represented by (Les) and times range from 2 weeks 14 months. Arrows represent most rostral extension of retrograde degeneration for each time period. Abbreviations : CP, cerebral peduncle; DecPyr, decussation of the pyramidal tract; G, gracile nucleus; IC, inferior colliculus; 10, inferior olivary nucleus; P, pontine nuclei; RN, red nucleus; SC, superior colliculus; Trap, trapezoid body.

only the giant cells are affected and not the 'ordinary large pyramids' of layer 5. Thus, they may have mistaken shrunken Betz cells for 'ordinary pyramids' and erroneously concluded that the giant pyramids had disappeared instead of merely shrinking as the present results indicate. Levin and Bradford 19 concluded that most (81 ~ ) of the giant cells were affected by chromatolysis 17 days after a monkey had undergone a spinal cord hemisection, and by 28 days there was severe cell loss. These alterations affected the ordinary large pyramids in area 4 as well as those in the neighboring somatosensory and parietal areas. Lasek is by contrast argued that although the Betz cells seemed to have vanished from the motor cortex of a monkey 28 days after a pyramidal tract lesion, there was no evidence of cellular disappearance such as gliosis, 'ghost cells', or partial atrophy. Thus, he believed that the Betz cells had uniformly decreased in magnitude owing primarily to a loss of Nissl substance. Similarly, the present study finds no evidence for chromatolysis, gliosis, 'ghost cells' or for cell loss, and we conclude that the pyramidal cells have simply shrunk.

The pyramidal tract When a nerve fiber is cut, its distal segment undergoes Wallerian degeneration; however, the fate of the proximal segment has long been a subject of controversy. Previous findings obtained in a number of different species and fiber systems and by various staining methods have variously suggested that (a) no retrograde axon change occurs, (b) the proximal segment degenerates over varying distances or (c) the axons undergo a slow atrophy. The controversy surrounding the question of retrograde axon degeneration is complex, primarily because of the many different staining meth-

24 ods employed, but also because of disagreements over what actually constitutes retrograde degeneration in a nerve fiber. In this discussion retrograde degeneration will be taken to mean argyrophilic fragmentation or beading of individual axons in the axon segment proximal to the lesion. In his review of retrograde changes in nerve fibers, Beresford 5 suggested that 'the diversity among retrograde cell atrophies offers the key to predicting the late of the proximal part of a cut fiber'. Thus retrograde axon degeneration can be considered in relation to (a) cell bodies which show chromatolytic changes but eventually recover, (b) those which undergo rapid degeneration and eventually disappear and (c) those which only partially atrophy. The recovery of the nerve cell body after axonal transection has been demonstrated, for example, in the ventral horn motor neurons of the spinal cord a,~ and this recovery is accompanied by the regeneration of the peripheral motor nerve. However, in other regions of the nervous system, where axonal regeneration does not occur, rapid cell death following section of the axon is a common phenomenon (see Cragg 1° for a review). A number of investigators have associated this rapid cell death with the degeneration of the proximal axon segment. Van Gehuchten 21 found that after transecting the Xth cranial nerve, and the rubro-, vestibulo-, and reticulo-spinal tracts in the rabbit 'indirect Wallerian degeneration' could be found in the proximal stump with the Marchi method 20-40 days afterwards, accompanied by rapid cell death in the nuclei of origin. Van Gehuchten stressed the importance of the term 'indirect Wallerian' as opposed to 'retrograde' degeneration because he believed that this degeneration began at the cell body and proceeded away from it, that it was Wallerian in nature and that it resulted directly from the rapid atrophy and death of the cell body. More recent studies have demonstrated retrograde fiber degeneration with the Nauta method. Cowan e t al. 9 found that beginning at 12 days after eye-enucleation in the pigeon there was retrograde fiber degeneration in the isthmo-optic tract. Because the fiber degeneration began close to the nucleus of origin, progressed rapidly in a centrifugal direction, and was accompanied by severe cell loss in the isthmo-optic nucleus, it could be classified as an indirect Wallerian degeneration. Guillery14 described retrograde degeneration in geniculo-cortical axons of the cat at survival times of 5-15 days. This reaction was accompanied by rapid cell degeneration in specific regions of the lateral geniculate nucleus. Grant and Aldskogiusla stained retrograde axon degeneration in the kitten hypoglossal nerve after 7 days survival. They, like Van Gehuchten, emphasized the term 'indirect Wallerian' to describe the fiber degeneration which began at the cell body of origin and presumably resulted from the rapid cell death which they observed in the hypoglossal nucleus. If we consider that the large pyramidal neurons in the motor cortex do not undergo rapid atrophy and death but remain in a steady shrunken state, then it is reasonable to expect that perhaps not all of the proximal axon segment will degenerate. However, it is surprising to find that previous studies have not demonstrated any retrograde degeneration in the pyramidal tract. Van Gehuchten 2t hemisected the rabbit spinal cord but after 30-60 days found no retrograde pyramidal tract degeneration with the Marchi method. Although he was ignorant of the fate of the cortical

25 cell bodies, Van Gehuchten argued somewhat circularly that the absence of 'indirect Wallerian degeneration' in the tract showed that the cortical cells must not have undergone a rapid atrophy. Lasek is, though he believed that the cortical cell bodies of rhesus monkeys had shrunk and not disappeared after survival times of 1,3, and 10 months, denied any loss, atrophy, or degeneration of the pyramidal axons above the lesion when the protargol silver method was used. Glees lz reached a similar conclusion, since after one year the Marchi method showed no retrograde pyramidal degeneration in the cat and rabbit. Tower 20 claimed that the Marchi method showed retrograde degeneration in the monkey's pyramidal tract but this was not a consistent result. Lance 17, using the Rogers silver method, claimed to have found retrograde axon degeneration in the cat's pyramidal tract, but actually described a loss of fibers. A recent study of retrograde axon degeneration s was undertaken in the medial lemniscus of the cat, another system where the nerve cell bodies do not appear to undergo rapid atrophy and death. With the Nauta-Gygax method, no retrograde drop-like disintegration could be demonstrated in the medial lemniscus up to one year after the lesion. In the gracile and cuneate nuclei, many cells showed a loss of Nissl substance and a marked shrinkage. Some apparent cell loss was also reported. The proximal axon segment of the lemniscal fibers decreased in diameter but maintained its structural integrity and normal staining qualities. A number of questions remain unanswered. First, what are the ultrastructural differences between anterograde and retrograde degeneration in a nerve fiber? Recently Aldskogiusl, 2 described electron microscopically the appearance of silverstained indirect and direct Wallerian degeneration in the kitten hypoglossal nerve after 1-5 days survival. He concluded that light microscopically the indirect degeneration is granular in appearance (after 6-21 days survival) whereas the direct Wallerian degeneration is seen as axonal fragments. At the electron microscopic level, the difference was attributed to short v e r s u s long myelinated electron-dense axoplasmic fragments, respectively, which would imply that in indirect Wallerian degeneration a nerve fiber breaks into shorter fragments. Although we have noted the somewhat granular appearance of retrograde fiber degeneration, we have also described beaded and fragmented axons proximal to the lesion. Thus, the retrograde degeneration in our material is likely to have a different ultrastructural appearance from the indirect Wallerian degeneration described by Aldskogius. Moreover, Aldskogius used immature animals in his experiments and in fact did not observe indirect Wallerian degeneration in the hypoglossal nerve of adult cats. Second, one would like to know what mechanism underlies the preservation of many of the pyramidal axons rostral to the pons as well as the partial preservation of the cortical cell body. The presence of sustaining collaterals has often been invoked to explain the preservation of these parts of the neuron after axotomy 7 but this theory would be difficult to prove. Finally, it would be of interest to know why, when the cell dies, the indirect Wallerian degeneration begins in the axonal region closest to the cell body, but when the cell only partially atrophies the retrograde degeneration begins in the axonal region closest to the lesion. This difference in progression of the axonal reactions as

26 well as the difference in their time course suggest that the two degenerative p h e n o m ena m a y have different underlying mechanisms. This review o f the literature reveals t h a t o u r d e m o n s t r a t i o n of' r e t r o g r a d e a x o n d e g e n e r a t i o n with a m o d e r n silver technique constitutes a new finding. Previous studies have d e m o n s t r a t e d an indirect W a l l e r i a n d e g e n e r a t i o n which progresses r a p i d l y in a cellulifugal direction a n d is caused by the d e a t h o f the cell. However, we wish to e m p h a s i z e t h a t o u r findings do not represent an indirect W a l l e r i a n degeneration because first, the cortical neurons do n o t die, a n d second, the d e g e n e r a t i o n p r o ceeds slowly from the lesion site t o w a r d s the cell b o d y but does n o t a p p e a r to p r o g r e s s a l o n g the entire p r o x i m a l axon segment. Indirect W a l l e r i a n d e g e n e r a t i o n , by contrast, begins at the cell b o d y o f origin a n d within several weeks e n c o m p a s s e s the entire axon p r o x i m a l to the lesion. Thus, the f r a g m e n t e d a n d b e a d e d a x o n s seen in o u r m a t e r i a l represent a true r e t r o g r a d e d e g e n e r a t i o n o f p y r a m i d a l t r a c t axons. M o r e o v e r . it a p p e a r s that the degenerative process reaches a p o i n t o f e q u i l i b r i u m at which a p a r t i a l l y s h r u n k e n p y r a m i d a l cell is m a i n t a i n i n g a p a r t i a l l y degenerated axon. ACKNOWLEDGEMENTS W e t h a n k Dr. R. W. G u i l l e r y for critical r e a d i n g o f the m a n u s c r i p t . 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 T r a i n i n g G r a n t GZ-2385 a n d a g r a n t f r o m the A l f r e d P. Sloan F o u n d a t i o n .

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!l 12

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27 13 GRANT, G., AND ALDSKOGIUS, H., Silver impregnation of degenerating dendrites, cells and axons central to axonal transection. 1. A Nauta study on the hypoglossal nerve in kittens, E.vp. Brain Res., 3 (1967) 150-162. 14 GUILLERY, R. W., Patterns of fiber degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in the visual cortex, I. comp. Neurol., 130 (1967) 197-222. 15 HOLMES,G., AND MAY, W. P., On the exact origin & t h e pyramidal tract in man and other man-,reals, Brain, 32 (1909) 1 43. 16 KALIL, K., Retrograde axon degeneration in the pyramidal tract of the hamster, Anat. Rec., 175 (1973) 352. 17 LANCE, J. W., Behavior of pyramidal axons following section, Brain, 77 (1954) 314-324. 18 LASEK, A. M., The pyramidal tract: a study of retrograde degeneration in the monkey, Arch. Neurol. Pa3'chiat. (Chic.), 48 (1942) 561-567. 19 LEVIN, P. M., AND BRADFORD, F. K., The exact origin of the corticospinal tract in the monkey, J. comp. Ncurol., 68 (1938)411 422. 20 TOWER, S. S., Pyramidal lesion in the monkey, Brain, 63 (1940) 36 90. 21 VAN GEHUCHTEN, A., La d6g6n6rescence dite r6trograde ou d6g6n6rescence Wall6rienne indirecte, Ndvraxe, 5 (1903) 1-108.

Retrograde cortical aand axonal changes following lesions of the pyramidal tract.

Following lesions of the pyramidal tract in hamsters, retrograde changes were studied in the sensorimotor cortex and in the pyramidal tract axons prox...
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