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Differences in proximal and distal conduction velocities of efferent nerve fibers to the medial gastrocnemius muscle
Brain Research, 91 (1975) 147-150 c@) Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
147
Differences in proximal and distal conduction velocities of efferent nerve fibers to the medial gastrocnemius muscle
PAULA B. COPACK, ERICA FELMAN, JAMES S. LIEBERMAN* AND SID GILMAN Department of Neurology, College of Physicians and Surgeons of Columbia University, New York, N. Y. 10032 (U.S.A.)
(Accepted March 10th, 1975)
Eccles and Sherrington 3 measured the diameters of efferent nerve fibers to the medial gastrocnemius (MG) muscle of chronically deafferented cats and found a bimodal distribution with peak values of 16 and 6 # m at a distance of 60 m m from the muscle. They ascribed this distribution to the existence of 2 separate unimodal populations rather than a single population of fibers which branch to form a bimodal population, since they observed a similar distribution in the ventral root where branching of nerve fibers does not occur 3. However, they found increasing total numbers of nerve fibers in sections progressively closer to the nerve-muscle junction and, in teased fiber preparations, they observed some motor nerve fibers undergoing branching. They concluded that m o t o r nerve fibers branch as they approach muscle and the rate of multiplication of fibers within nerve progressively increases with approach to muscle. Subsequent studies have confirmed these findings and demonstrated that, in general, fibers showing peak diameters of 16 and 6 # m correspond to alpha-motor and fusimotor fibers, respectively4-6, s. However, owing to the fact that large diameter fibers usually divide into smaller diameter branches, at sections of nerve close to muscle, many small diameter fibers are likely to be branches of alpha-motor fibers rather than fusimotor fibers. Anatomical evidence suggests that alpha-motor fibers branch to a greater extent than fusimotor fibers1, 3. Muscle afferent fibers also branch near the nerve-muscle junction 3. Electrophysiological studies of the conduction velocities of single afferent fibers have shown that slowing of conduction occurs over the distal segment of a large proportion of fibers 7. Similar studies have not been carried out on efferent fibers. In the present study, conduction velocities (CVs) of efferent fibers to the M G muscle were measured to determine (1) what proportion of efferent fibers branch as indicated by a change in CV over 2 segments (proximal and distal) of the nerve, (2) whether by physiological means we could confirm the fact that alpha-motor fibers branch to a greater degree than fusimotor fibers, (3) how large an 'error '2 occurs in the * Present address: Department of Neurology, University of California at Davis, Davis, Calif. 95616, U.S.A.
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CV PROXIMAL ( M / s e e ]
Fig. 1. Histogram of distributions of proximal conduction velocities of efferent fibers to medial gastrocnemius muscle.
estimation of CV when measurements taken near the muscle are compared with those at a distance from the muscle and (4) whether alpha-motor fibers with faster CVs show a greater slowing of conduction approaching the muscle than alpha-motor fibers with slower CVs. Cats were anesthetized with sodium pentobarbital 30 mg/kg and maintained throughout surgery and recording on supplementary doses of 2 mg as needed for deep anesthesia. After tracheal and venous cannulation, a laminectomy was performed to expose ventral roots L7 and $1. The left M G muscle was separated from surrounding tissues; the proximal attachments, vascular and nerve supplies were preserved. Nerves to the lateral gastrocnemius, plantaris, soleus, posterior tibial and anterior tibial muscles were severed. Two pairs of Ag-AgC1 stimulating electrodes were positioned on the M G nerve at an intercathodal distance of about 20 mm with the distal electrode next to the junction of nerve and muscle. The ventral root which showed the largest amplitude response to electrical stimulation of M G nerve, usually $1, was severed at its exit from the spinal cord and placed on a dissection plate. Dissected tissues of the cord and hindlimb were covered with mineral oil equilibrated with 95 ~ 02-5 ~ COz. Temperatures of the pools and body (rectum) were maintained at 37 °C. Ventral root fibers were dissected repeatedly until single units could be identified by antidromic stimulation of the M G nerve. Latencies were measured in response to stimuli applied through proximal and distal stimulation sites at twice threshold intensity. At the termination of each experiment the entire neural segment from ventral root to M G nerve was removed and placed on paper without stretching. Distances from recording site to proximal and distal stimulation sites were measured. Conduction velocities were computed for the proximal segment by dividing the distance from proximal cathode to recording electrode by the latency to onset of the response. Conduction velocities were computed for the distal segment by dividing the distance between stimulation cathodes by the differences in latencies obtained from responses to stimuli delivered through the proximal and distal electrodes. A value of 0.1 msec was deducted from latency values
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CV DISTAL ( l i l l s e ¢ )
Fig. 2. Conduction velocity of single efferent fibers to the medial gastrocnemius muscle, showing the relationship of proximal (ordinate) to distal (abscissa) conduction velocity.
for utilization time. A total of 61 units was recorded, but data from 10 were rejected because of injury to the fibers as shown by a gradual decrease in amplitude of the unit during the recording session, an extremely fast CV and a high threshold for stimulation. A histogram of the distribution of CVs of the remaining 51 units across the proximal segment revealed a bimodal distribution (Fig. 1). Eleven units had CVs below 55 MPS across the proximal segment and thus represent activity in fusimotor fibersS; the remaining units had higher CVs and thus represent activity conducted in alpha-motor fibers. In Fig. 2, CVs of single fibers measured across the proximal segment are plotted against CVs measured over the distal segment for both alpha-motor and fusimotor fibers. Forty-four of 51 points (86 ~ ) fall above a reference line drawn to pass through the origin at 45 ° and thus represent units with CVs greater proximally than distally. Nine of 11 (82 ~ ) of the fusimotor fibers show faster CVs over the proximal segment and 35 of 40 (88 ~ ) alpha-motor fibers show greater proximal than distal CVs. Some of the alpha-motor units show marked differences in CV across the 2 segments, with much slower CVs across the distal segment. Examination of these data with a Wilcoxon Rank Sum Test shows that CVs over the proximal segment are significantly greater than those over the distal segment (for fusimotor fibers, P < 0.05; for alphamotor fibers, P < 0.001). Comparison of fusimotor with alpha-motor CVs using the Wilcoxon Rank Sum Test reveals that alpha-motor fibers show a significantly (P < 0.05) greater decrease in CV approaching muscle, indicating that alpha-motor fibers branch to a greater degree than fusimotor fibers. Ebel and Gilman 2 used the data of Eccles and Sherrington 3 for fiber branching to derive a theoretical mathematical expression for expected 'error' in measurement of CV from ventral root to a site 10 mm from the M G muscle as compared with the CV measured from ventral root to a site 50 mm from the muscle. The error they described,
150 an expected average per cent decrease in conduction velocity due to branching, was 7 ~. We compared our experimental data with these theoretical data by subtracting CVs over the entire conduction distance from the proximal CVs and dividing the differences by the proximal CVs. The result was an average per cent difference of 4 (range 1-7 ~), a value close to that predicted by Ebel and Gilman. Thus, the CV of a particular nerve fiber varies as a function of the distance over which the CV is measured and the site of recording. Branching does not occur in ventral roots s; it is slight in the nerve segment immediately extradural, and becomes progressively greater as nerve approaches muscle 3. Consequently, recordings from nerve fibers close to the nerve-muscle junction are likely to be made from branches of parent fibers rather than the parent fibers themselves. The relationship of proximal CV to the difference between proximal and distal CV for individual fibers was examined using Spearman's Rank Correlation Test. The result (0.1) was not significant, indicating no correlation between proximal CV and degree of slowing distally. In addition, inspection of data in Fig. 2 reveals that some fibers with rapid CVs proximally show slow CVs distally indicating that branching had occurred. Others show no decrease in CV over the distal segment indicating that little or no branching had occurred. We conclude that there is a decrease of conduction velocity near the nervemuscle junction of 86 ~ of the single axons studied. The data indicate that the proportion of alpha-motor fibers showing a distal decrease of CV is approximately equal to that of fusimotor fibers, but that the degree of change in velocity distally is considerably greater for alpha-motor fibers. The present experimental data concerning the per cent change in conduction velocity over distal nerve segments agree with the theoretical results of Ebel and Gilman 2 indicating an expected average 'error' of 4 ~. Within the alpha-motor fiber group there is no relationship between proximal CV and the degree of decrease in CV distally. This work was supported in part by US Public Health Service Grants NS 52431, NS 05184, and NS 10612. 1 ADAL,M. N., AND BARKER,D., Intramuscular branching of fusimotor fibres, J. Physiol. (Lond.), 177 (1965) 288-299. 2 EBEL, H. C., AND GILMAN, S., Estimation of errors in conduction velocity measurements due to branching of peripheral nerve fibers, Brain Research, 16 (1969) 273-276. 3 ECCLES,J. C., AND SHERRINGTON,C. S., Numbers and contraction-values of individual motor-units examined in some muscles of the limb, Proc. roy. Soc. B, 106 (1930) 326-357. 4 HURSH, J. B., Conduction velocity and diameter of nerve fibers, Amer. J. Physiol., 127 (1939) 131-139. 5 KUFFLER, S. W., HUNT, C. C., AND QUILLIAM,J. P., Function of medullated small-nerve fibers in mammalian ventral roots: efferent muscle spindle innervation, J. Neurophysiol., 14 (1951) 29-54. 6 LEKSELL,L., The action potential and excitatory effects of the small ventral root fibers to skeletal muscle, Actaphysiol. scand., 10, Suppl. 31 (1945) 1-84. 7 MCDONALD, W. ]., AND GILMAN, S., Demyelination and muscle spindle function. Effect of diphtheritic polyneuritis on nerve conduction and muscle spindle function in the cat, Arch. Neurol. (Chic.), 18 (1968) 508-519. 8 REXED,B., Contributions to the knowledge of the post-natal development of the peripheral nervous system in man, Acta psychiat. (Kbh.), Suppl. 33 (1944) 1-206.
147
Differences in proximal and distal conduction velocities of efferent nerve fibers to the medial gastrocnemius muscle
PAULA B. COPACK, ERICA FELMAN, JAMES S. LIEBERMAN* AND SID GILMAN Department of Neurology, College of Physicians and Surgeons of Columbia University, New York, N. Y. 10032 (U.S.A.)
(Accepted March 10th, 1975)
Eccles and Sherrington 3 measured the diameters of efferent nerve fibers to the medial gastrocnemius (MG) muscle of chronically deafferented cats and found a bimodal distribution with peak values of 16 and 6 # m at a distance of 60 m m from the muscle. They ascribed this distribution to the existence of 2 separate unimodal populations rather than a single population of fibers which branch to form a bimodal population, since they observed a similar distribution in the ventral root where branching of nerve fibers does not occur 3. However, they found increasing total numbers of nerve fibers in sections progressively closer to the nerve-muscle junction and, in teased fiber preparations, they observed some motor nerve fibers undergoing branching. They concluded that m o t o r nerve fibers branch as they approach muscle and the rate of multiplication of fibers within nerve progressively increases with approach to muscle. Subsequent studies have confirmed these findings and demonstrated that, in general, fibers showing peak diameters of 16 and 6 # m correspond to alpha-motor and fusimotor fibers, respectively4-6, s. However, owing to the fact that large diameter fibers usually divide into smaller diameter branches, at sections of nerve close to muscle, many small diameter fibers are likely to be branches of alpha-motor fibers rather than fusimotor fibers. Anatomical evidence suggests that alpha-motor fibers branch to a greater extent than fusimotor fibers1, 3. Muscle afferent fibers also branch near the nerve-muscle junction 3. Electrophysiological studies of the conduction velocities of single afferent fibers have shown that slowing of conduction occurs over the distal segment of a large proportion of fibers 7. Similar studies have not been carried out on efferent fibers. In the present study, conduction velocities (CVs) of efferent fibers to the M G muscle were measured to determine (1) what proportion of efferent fibers branch as indicated by a change in CV over 2 segments (proximal and distal) of the nerve, (2) whether by physiological means we could confirm the fact that alpha-motor fibers branch to a greater degree than fusimotor fibers, (3) how large an 'error '2 occurs in the * Present address: Department of Neurology, University of California at Davis, Davis, Calif. 95616, U.S.A.
148
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CV PROXIMAL ( M / s e e ]
Fig. 1. Histogram of distributions of proximal conduction velocities of efferent fibers to medial gastrocnemius muscle.
estimation of CV when measurements taken near the muscle are compared with those at a distance from the muscle and (4) whether alpha-motor fibers with faster CVs show a greater slowing of conduction approaching the muscle than alpha-motor fibers with slower CVs. Cats were anesthetized with sodium pentobarbital 30 mg/kg and maintained throughout surgery and recording on supplementary doses of 2 mg as needed for deep anesthesia. After tracheal and venous cannulation, a laminectomy was performed to expose ventral roots L7 and $1. The left M G muscle was separated from surrounding tissues; the proximal attachments, vascular and nerve supplies were preserved. Nerves to the lateral gastrocnemius, plantaris, soleus, posterior tibial and anterior tibial muscles were severed. Two pairs of Ag-AgC1 stimulating electrodes were positioned on the M G nerve at an intercathodal distance of about 20 mm with the distal electrode next to the junction of nerve and muscle. The ventral root which showed the largest amplitude response to electrical stimulation of M G nerve, usually $1, was severed at its exit from the spinal cord and placed on a dissection plate. Dissected tissues of the cord and hindlimb were covered with mineral oil equilibrated with 95 ~ 02-5 ~ COz. Temperatures of the pools and body (rectum) were maintained at 37 °C. Ventral root fibers were dissected repeatedly until single units could be identified by antidromic stimulation of the M G nerve. Latencies were measured in response to stimuli applied through proximal and distal stimulation sites at twice threshold intensity. At the termination of each experiment the entire neural segment from ventral root to M G nerve was removed and placed on paper without stretching. Distances from recording site to proximal and distal stimulation sites were measured. Conduction velocities were computed for the proximal segment by dividing the distance from proximal cathode to recording electrode by the latency to onset of the response. Conduction velocities were computed for the distal segment by dividing the distance between stimulation cathodes by the differences in latencies obtained from responses to stimuli delivered through the proximal and distal electrodes. A value of 0.1 msec was deducted from latency values
149
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CV DISTAL ( l i l l s e ¢ )
Fig. 2. Conduction velocity of single efferent fibers to the medial gastrocnemius muscle, showing the relationship of proximal (ordinate) to distal (abscissa) conduction velocity.
for utilization time. A total of 61 units was recorded, but data from 10 were rejected because of injury to the fibers as shown by a gradual decrease in amplitude of the unit during the recording session, an extremely fast CV and a high threshold for stimulation. A histogram of the distribution of CVs of the remaining 51 units across the proximal segment revealed a bimodal distribution (Fig. 1). Eleven units had CVs below 55 MPS across the proximal segment and thus represent activity in fusimotor fibersS; the remaining units had higher CVs and thus represent activity conducted in alpha-motor fibers. In Fig. 2, CVs of single fibers measured across the proximal segment are plotted against CVs measured over the distal segment for both alpha-motor and fusimotor fibers. Forty-four of 51 points (86 ~ ) fall above a reference line drawn to pass through the origin at 45 ° and thus represent units with CVs greater proximally than distally. Nine of 11 (82 ~ ) of the fusimotor fibers show faster CVs over the proximal segment and 35 of 40 (88 ~ ) alpha-motor fibers show greater proximal than distal CVs. Some of the alpha-motor units show marked differences in CV across the 2 segments, with much slower CVs across the distal segment. Examination of these data with a Wilcoxon Rank Sum Test shows that CVs over the proximal segment are significantly greater than those over the distal segment (for fusimotor fibers, P < 0.05; for alphamotor fibers, P < 0.001). Comparison of fusimotor with alpha-motor CVs using the Wilcoxon Rank Sum Test reveals that alpha-motor fibers show a significantly (P < 0.05) greater decrease in CV approaching muscle, indicating that alpha-motor fibers branch to a greater degree than fusimotor fibers. Ebel and Gilman 2 used the data of Eccles and Sherrington 3 for fiber branching to derive a theoretical mathematical expression for expected 'error' in measurement of CV from ventral root to a site 10 mm from the M G muscle as compared with the CV measured from ventral root to a site 50 mm from the muscle. The error they described,
150 an expected average per cent decrease in conduction velocity due to branching, was 7 ~. We compared our experimental data with these theoretical data by subtracting CVs over the entire conduction distance from the proximal CVs and dividing the differences by the proximal CVs. The result was an average per cent difference of 4 (range 1-7 ~), a value close to that predicted by Ebel and Gilman. Thus, the CV of a particular nerve fiber varies as a function of the distance over which the CV is measured and the site of recording. Branching does not occur in ventral roots s; it is slight in the nerve segment immediately extradural, and becomes progressively greater as nerve approaches muscle 3. Consequently, recordings from nerve fibers close to the nerve-muscle junction are likely to be made from branches of parent fibers rather than the parent fibers themselves. The relationship of proximal CV to the difference between proximal and distal CV for individual fibers was examined using Spearman's Rank Correlation Test. The result (0.1) was not significant, indicating no correlation between proximal CV and degree of slowing distally. In addition, inspection of data in Fig. 2 reveals that some fibers with rapid CVs proximally show slow CVs distally indicating that branching had occurred. Others show no decrease in CV over the distal segment indicating that little or no branching had occurred. We conclude that there is a decrease of conduction velocity near the nervemuscle junction of 86 ~ of the single axons studied. The data indicate that the proportion of alpha-motor fibers showing a distal decrease of CV is approximately equal to that of fusimotor fibers, but that the degree of change in velocity distally is considerably greater for alpha-motor fibers. The present experimental data concerning the per cent change in conduction velocity over distal nerve segments agree with the theoretical results of Ebel and Gilman 2 indicating an expected average 'error' of 4 ~. Within the alpha-motor fiber group there is no relationship between proximal CV and the degree of decrease in CV distally. This work was supported in part by US Public Health Service Grants NS 52431, NS 05184, and NS 10612. 1 ADAL,M. N., AND BARKER,D., Intramuscular branching of fusimotor fibres, J. Physiol. (Lond.), 177 (1965) 288-299. 2 EBEL, H. C., AND GILMAN, S., Estimation of errors in conduction velocity measurements due to branching of peripheral nerve fibers, Brain Research, 16 (1969) 273-276. 3 ECCLES,J. C., AND SHERRINGTON,C. S., Numbers and contraction-values of individual motor-units examined in some muscles of the limb, Proc. roy. Soc. B, 106 (1930) 326-357. 4 HURSH, J. B., Conduction velocity and diameter of nerve fibers, Amer. J. Physiol., 127 (1939) 131-139. 5 KUFFLER, S. W., HUNT, C. C., AND QUILLIAM,J. P., Function of medullated small-nerve fibers in mammalian ventral roots: efferent muscle spindle innervation, J. Neurophysiol., 14 (1951) 29-54. 6 LEKSELL,L., The action potential and excitatory effects of the small ventral root fibers to skeletal muscle, Actaphysiol. scand., 10, Suppl. 31 (1945) 1-84. 7 MCDONALD, W. ]., AND GILMAN, S., Demyelination and muscle spindle function. Effect of diphtheritic polyneuritis on nerve conduction and muscle spindle function in the cat, Arch. Neurol. (Chic.), 18 (1968) 508-519. 8 REXED,B., Contributions to the knowledge of the post-natal development of the peripheral nervous system in man, Acta psychiat. (Kbh.), Suppl. 33 (1944) 1-206.