408
Brain Research, 167 (1979) 408 411 t', Elsevier/North-Holland Biomedical Press
Left cortical lesion and soleus muscle sarcomere number
A. HAYAT, C. TARDIEU and C. TABARY*
FRA 18. I N S E R M . Hdpital Raymond Poincar~. 92380 Garches France
If after left cortical lesion in somatosensory I areas both solei were immobilized 7 days in the shortened position, a bilateral decrease (50 %) in sarcomere number was measured. In immobilized control group the decrease was 40 %. The latter decrease was found for lesions elsewhere than in S 1. A possible influence of the central nervous system on hypoextensibility of skeletal muscles was investigated. Hypoextensibility ('contracture') is an increased passive resistance to extension of the non-contracting muscle. Schaltenbrand 6 failed to find abnormal contraction or hypoextensibility of muscles after unilateral decortication. Spiegel 7 found 'contracture' after removal of the left m o t o r cortex in cat immobilized extensor muscles in shortened position. However, lack of control experiments reduced the significance of this finding. Because hypoextensibility and reduction in sarcomere number were found in immobilized shortened soleusL it was then interesting to compare the effect of the same immobilization after unilateral lesion of motor cortex. Four groups of adult cats were used: In the first 9 cats had a cerebral lesion in somatosensory I. Seven days later, both solei were immobilized in the shortened position for 7 days by plaster casts. In the second 9 cats had the same immobilization. Thirdly, 5 cats had lesions without immobilization. And in the fourth. 5 cats had lesions elsewhere than in S I plus immobilization. Cats were anesthetized with pentobarbitone (30 mg/kg). The skull was opened and lesion made by means of a Pasteur pipette. Two days later, placing reaction of the hind limbs was checked every day. At the end of the experience a clinical or dynamographic 9 measurement of soleus hypoextensibility was made, the sciatic nerve and the synergist gastrocnemius being cut. For the soleus muscle the sarcomere number of single fibers was evaluated using the Close method 1. Results were expres~d by the ratio of experimental sarcomere number to an experimentally a estimated normal number. The brain was fixed and photographs of the lesion were taken. Left hemisphere was embedded in Agar (5 %) and sliced Sample t-test was applied to the intra and inter-groups comparisons. In group I the absence of placing reaction was found in the contratateral hind * This research was supported by | N S E R M (Paris) (Grant 38-76-70-006)
409
!
~0
/
/ , I // 1/ /"
0N
z: ~J /
50(
j
•/// ,,
.,,i
,.*
/ / /o s / / - ~,,° /;%
I.e~ .-.
.-. m..
-"
I.-
lmm
...................
~
EXTENSION
ANKLE-ANGLE 120
90
60
Fig. 1. Plot of passive tension against extension of a normal soleus (dotted line) and left and right soleus muscles (broken lines) of one cat from group i having lost 50 ~ sarcomeres. For a given ankle angle, the tension is stronger for the experimental muscle than for the normal one. limb. A weak resistance for an ankle angle of 155-110 ° demonstrated a strong hypoextensibility. Fig. I shows passive tension-extension curves. Sarcomere number ratios were 0.49 ~ 0.02 and 0.50 ~ 0.02 for the left and the right solei. These results were not significantly different. Fig. 2 shows the surface photograph of the lesion. Frontal, lateral and depth coordinates of the lesion were measured for every cut and standardized volumes estimated. They were not too different. In group II, hypoextensibility was marked (125-100°). Ratios were 0.62 ± 0.05 and 0.64 ~ 0.04 without significant difference beLween left and right muscles. In group III, where the lesion was similar to group !, placing reaction was absent for the contralateral hind limb. There was no hypoextensibility. Ratios were 0.97 0.02 and 0.98 ± 0.02. In group IV, hypoextensibility was evident (125-110 °) and ratios were 0.60 0.05 and 0.59 ± 0.04. Inter-groups comparisons. Significant differences were found between groups I and II for the left and for the right soleus (P < 0.05 and P < 0.01). No significant difference was found between groups IV and II and between group III and normal animals. In our experimental animals with lesions and without immobilization (III), walking and even running were observed without any hypoextensibility of the soleus. The sarcomere number within the single soleus fiber was found to be normal. Reduction of sarcomeres (40 ~o) is important within 7 days for the control group (lI). Under the same conditions, reduction o f sarcomeres was o f 50 ~ for the lesion group (I). The influence of the lesion is then distinguished. In the two groups, hypoextensibilities o f the muscle are observed in the absence of any contraction. Some hypothesis about the possible origin o f this difference between control and lesion groups may be done: Lundberg 5 reported the suppression of the inhibition on the extensor muscles by frontal lesion. On the other hand frequent contractions of the soleus are one of the
410
Coordinates [mmJ Right gyrus Left lesion Frontal 5
Frontal 4-9.8
Estimated volume t Lateral 0.2-0.6
Depth 2.6-3.4
110
Fig. 2. Localized lesion in left somatosensory I. A : surface photograph. The frontal coor~ gyrus of the right intact hemisphere is measured as a reference. B: one of the transversal cut o hemisphere (scale -- 1 ram). Lesion is identified by hemostatic spongel.
f a c t o r s r e g u l a t i n g s a r c o m e r e n u m b e r , this is s u p p o r t e d
by i n v e s t i g a t i o n s d
locally t e t a n i z e d m u s c l e s 4. It is n o t i c e a b l e t h a t lesion effect leads to f u r t h e r decJ s a r c o m e r e n u m b e r , w h i l e d e n e r v a t i o n acts in t h e o p p o s i t e d i r e c t i o n L Lesiot m e a s u r e d by s t e r e o t a x i c c o o r d i n a t e s in S I. R e f e r e n c e to H a s s l e r ' s 3 c y t o a r c h i t s t u d y w o u l d s u g g e s t a p o s s i b l e l o c a l i z a t i o n in areas 4 and 6. H o w e v e r . t h e s z a t i o n o f S I t h r o u g h t h e p r e s e n t s t u d y is s u g g e s t e d by g r o u p I V (lesions mad, a u d i t o r y , visual a n d o r b i t a l c o r t e x ) a n d its effects w e r e n o t different to that c o n t r o l g r o u p II. I n t h e p r e s e n t s t u d y t h e S I t y p e o f lesion is d e m o n s t r a t e d t o I influence o n b o t h solei w h e n i m m o b i l i z e d in s h o r t e n e d p o s i t i o n . I Close. R., Dynamic properties of fast and slow muscles of the rat during development, ,/. (Lond.), 173 (1964) 74-95. 2 Hayat, A., Tardieu, C., Tabary J. C. and Tabary, C. Effects of denervation on the s~ number of the soleus immobilized in the shortened position, J. Physiol. (Paris), 74 (1978) 3 Hassler, R., und Muhs-Clement, K., Architektonisher Aufbau des sensomotorisci parietalen Cortex der Katze, J. Hirnforsch., 6 (t964) 377-424. 4 Huet de la Tour, E., Tardieu, C., Tabary, J. C. and Tabary, C., Decrease of muscle ext< and reduction of sarcomere number in soteus muscle following a local injection of tetanus J. Neurol. Sci.. 40 (1979). 5 Lundberg, A., Interaction entre voles r6flexes spinales, Acta neurophysiol., 6 (1965) 120-
411 6 Schaltenbrand, G., and Cobb, S., Clinical and anatomical studies on two cats without neocortex, Brain, 53 (1931) 449~488. 7 Spiegel, E. A., und Shiboya, Die Bedeutung des Zentralnervensystems ffir die Entstehung muskul~rer Contracturen an singegipsten Extremit~iten, Z. ges. exp. Med., 44 (1924) 729-734. 8 Tabary, J. C., Tardieu, C., Tardieu, G., Tabary, C. and Gagnard, L., Functional adaptation of sarcomere number of normal cat muscle, J. Physiol. (Paris), 72 (1976) 277 291. 9 Tabary, J. C., Tabary, C., Tardieu, C., Tardieu, G., and Goldspink, G., Physiological and structural changes in the cat's soleus muscle due to immobilization at different lengths by plaster casts, J. Physiol. (Lond.), 224 (1972) 231-244.
Brain Research, 167 (1979) 408 411 t', Elsevier/North-Holland Biomedical Press
Left cortical lesion and soleus muscle sarcomere number
A. HAYAT, C. TARDIEU and C. TABARY*
FRA 18. I N S E R M . Hdpital Raymond Poincar~. 92380 Garches France
If after left cortical lesion in somatosensory I areas both solei were immobilized 7 days in the shortened position, a bilateral decrease (50 %) in sarcomere number was measured. In immobilized control group the decrease was 40 %. The latter decrease was found for lesions elsewhere than in S 1. A possible influence of the central nervous system on hypoextensibility of skeletal muscles was investigated. Hypoextensibility ('contracture') is an increased passive resistance to extension of the non-contracting muscle. Schaltenbrand 6 failed to find abnormal contraction or hypoextensibility of muscles after unilateral decortication. Spiegel 7 found 'contracture' after removal of the left m o t o r cortex in cat immobilized extensor muscles in shortened position. However, lack of control experiments reduced the significance of this finding. Because hypoextensibility and reduction in sarcomere number were found in immobilized shortened soleusL it was then interesting to compare the effect of the same immobilization after unilateral lesion of motor cortex. Four groups of adult cats were used: In the first 9 cats had a cerebral lesion in somatosensory I. Seven days later, both solei were immobilized in the shortened position for 7 days by plaster casts. In the second 9 cats had the same immobilization. Thirdly, 5 cats had lesions without immobilization. And in the fourth. 5 cats had lesions elsewhere than in S I plus immobilization. Cats were anesthetized with pentobarbitone (30 mg/kg). The skull was opened and lesion made by means of a Pasteur pipette. Two days later, placing reaction of the hind limbs was checked every day. At the end of the experience a clinical or dynamographic 9 measurement of soleus hypoextensibility was made, the sciatic nerve and the synergist gastrocnemius being cut. For the soleus muscle the sarcomere number of single fibers was evaluated using the Close method 1. Results were expres~d by the ratio of experimental sarcomere number to an experimentally a estimated normal number. The brain was fixed and photographs of the lesion were taken. Left hemisphere was embedded in Agar (5 %) and sliced Sample t-test was applied to the intra and inter-groups comparisons. In group I the absence of placing reaction was found in the contratateral hind * This research was supported by | N S E R M (Paris) (Grant 38-76-70-006)
409
!
~0
/
/ , I // 1/ /"
0N
z: ~J /
50(
j
•/// ,,
.,,i
,.*
/ / /o s / / - ~,,° /;%
I.e~ .-.
.-. m..
-"
I.-
lmm
...................
~
EXTENSION
ANKLE-ANGLE 120
90
60
Fig. 1. Plot of passive tension against extension of a normal soleus (dotted line) and left and right soleus muscles (broken lines) of one cat from group i having lost 50 ~ sarcomeres. For a given ankle angle, the tension is stronger for the experimental muscle than for the normal one. limb. A weak resistance for an ankle angle of 155-110 ° demonstrated a strong hypoextensibility. Fig. I shows passive tension-extension curves. Sarcomere number ratios were 0.49 ~ 0.02 and 0.50 ~ 0.02 for the left and the right solei. These results were not significantly different. Fig. 2 shows the surface photograph of the lesion. Frontal, lateral and depth coordinates of the lesion were measured for every cut and standardized volumes estimated. They were not too different. In group II, hypoextensibility was marked (125-100°). Ratios were 0.62 ± 0.05 and 0.64 ~ 0.04 without significant difference beLween left and right muscles. In group III, where the lesion was similar to group !, placing reaction was absent for the contralateral hind limb. There was no hypoextensibility. Ratios were 0.97 0.02 and 0.98 ± 0.02. In group IV, hypoextensibility was evident (125-110 °) and ratios were 0.60 0.05 and 0.59 ± 0.04. Inter-groups comparisons. Significant differences were found between groups I and II for the left and for the right soleus (P < 0.05 and P < 0.01). No significant difference was found between groups IV and II and between group III and normal animals. In our experimental animals with lesions and without immobilization (III), walking and even running were observed without any hypoextensibility of the soleus. The sarcomere number within the single soleus fiber was found to be normal. Reduction of sarcomeres (40 ~o) is important within 7 days for the control group (lI). Under the same conditions, reduction o f sarcomeres was o f 50 ~ for the lesion group (I). The influence of the lesion is then distinguished. In the two groups, hypoextensibilities o f the muscle are observed in the absence of any contraction. Some hypothesis about the possible origin o f this difference between control and lesion groups may be done: Lundberg 5 reported the suppression of the inhibition on the extensor muscles by frontal lesion. On the other hand frequent contractions of the soleus are one of the
410
Coordinates [mmJ Right gyrus Left lesion Frontal 5
Frontal 4-9.8
Estimated volume t Lateral 0.2-0.6
Depth 2.6-3.4
110
Fig. 2. Localized lesion in left somatosensory I. A : surface photograph. The frontal coor~ gyrus of the right intact hemisphere is measured as a reference. B: one of the transversal cut o hemisphere (scale -- 1 ram). Lesion is identified by hemostatic spongel.
f a c t o r s r e g u l a t i n g s a r c o m e r e n u m b e r , this is s u p p o r t e d
by i n v e s t i g a t i o n s d
locally t e t a n i z e d m u s c l e s 4. It is n o t i c e a b l e t h a t lesion effect leads to f u r t h e r decJ s a r c o m e r e n u m b e r , w h i l e d e n e r v a t i o n acts in t h e o p p o s i t e d i r e c t i o n L Lesiot m e a s u r e d by s t e r e o t a x i c c o o r d i n a t e s in S I. R e f e r e n c e to H a s s l e r ' s 3 c y t o a r c h i t s t u d y w o u l d s u g g e s t a p o s s i b l e l o c a l i z a t i o n in areas 4 and 6. H o w e v e r . t h e s z a t i o n o f S I t h r o u g h t h e p r e s e n t s t u d y is s u g g e s t e d by g r o u p I V (lesions mad, a u d i t o r y , visual a n d o r b i t a l c o r t e x ) a n d its effects w e r e n o t different to that c o n t r o l g r o u p II. I n t h e p r e s e n t s t u d y t h e S I t y p e o f lesion is d e m o n s t r a t e d t o I influence o n b o t h solei w h e n i m m o b i l i z e d in s h o r t e n e d p o s i t i o n . I Close. R., Dynamic properties of fast and slow muscles of the rat during development, ,/. (Lond.), 173 (1964) 74-95. 2 Hayat, A., Tardieu, C., Tabary J. C. and Tabary, C. Effects of denervation on the s~ number of the soleus immobilized in the shortened position, J. Physiol. (Paris), 74 (1978) 3 Hassler, R., und Muhs-Clement, K., Architektonisher Aufbau des sensomotorisci parietalen Cortex der Katze, J. Hirnforsch., 6 (t964) 377-424. 4 Huet de la Tour, E., Tardieu, C., Tabary, J. C. and Tabary, C., Decrease of muscle ext< and reduction of sarcomere number in soteus muscle following a local injection of tetanus J. Neurol. Sci.. 40 (1979). 5 Lundberg, A., Interaction entre voles r6flexes spinales, Acta neurophysiol., 6 (1965) 120-
411 6 Schaltenbrand, G., and Cobb, S., Clinical and anatomical studies on two cats without neocortex, Brain, 53 (1931) 449~488. 7 Spiegel, E. A., und Shiboya, Die Bedeutung des Zentralnervensystems ffir die Entstehung muskul~rer Contracturen an singegipsten Extremit~iten, Z. ges. exp. Med., 44 (1924) 729-734. 8 Tabary, J. C., Tardieu, C., Tardieu, G., Tabary, C. and Gagnard, L., Functional adaptation of sarcomere number of normal cat muscle, J. Physiol. (Paris), 72 (1976) 277 291. 9 Tabary, J. C., Tabary, C., Tardieu, C., Tardieu, G., and Goldspink, G., Physiological and structural changes in the cat's soleus muscle due to immobilization at different lengths by plaster casts, J. Physiol. (Lond.), 224 (1972) 231-244.
