Brain Research, 120 (1977) 179-183
179
© Elsevier/North-HollandBiomedicalPress, Amsterdam- Printed in The Netherlands
Velocity of supraspinal input and conduction velocity of axons of spinal motoneurons
TERRY C. PELLMARand G. G. SOMJEN Department o f Physiology and Pharmacology, Duke University, Durham, N.C. 27710 (U.S.A.)
(Accepted October 14th, 1976)
Based on their observations of reflexes, Sherrington and his associatesa inferred that red muscles were involved primarily in sustained postural contractions while pale muscles were used in fast voluntary movements. Further investigation1,11,1a has shown that within mixed muscles, pale fibers contract quickly and are innervated by large motoneurons with fast axons, whereas red fibers contract more slowly and receive input from smaller, more slowly conducting motoneurons. One might expect motor units of different time characteristics to be activated in a selective manner according to the temporal requirements of the movement. If so, then large motoneurons should be accessible to faster signals from supraspinal structures than smaller motoneurons. The time taken in the conduction and transmission of impulses is, of course, of little consequence for steadily maintained contraction but may well be significant for the accurate timing of phasic movements. Time requirements of inhibition would be similar to those of excitation. A positive correlation could therefore be expected between the latency of synaptic potentials evoked by stimulation of descending pathways and the latency of antidromic invasion of motoneurons in response to stimulation of their axons. It should be emphasized that it is the total time required for a signal to travel from the b:ain to the spinal motoneuron which is important for the testing of this hypothesis and not just the conduction velocity of the descending fibers. An analogous correlation has been observed between velocities of input to and output from lateral geniculate neurons in the visual pathway7. We have recorded antidromically conducted action potentials of motoneurons in the lumbosacral spinal cord of cats and the synaptic potentials evoked by way of the corticospinal and rubrospinal tracts. Experiments were conducted on 23 animals; 19 under chloralose anesthesia (initially 40-50 mg/kg body wt., i.v.); two under Nembutal anesthesia and two unanesthetized functionally decerebrate. In 11 of the anesthetized animals, the medulla oblongata was transected sparing only the pyramidsL Forked stimulating electrodes with interpolar distance of 1 mm were inserted into the right pyramidal tract, rostral to the plane of transection. In the 10 other anesthetized animals the brain stem remained intact; similar stimulating electrodes were placed in the pyramidal tract and concentric electrodes were placed in the right nucleus ruber.
180 Placement of the pyramidal tract electrode was guided by observing the antidromic evoked potential recorded from primary motor cortex. Following each experiment, the electrode placements and the transections were histologically verified. It found unsatisfactory, data were rejected. The lumbosacral spinal cord was exposed by laminectomy. Dorsal roots on the left side of L6-SI segments were cut. The left sciatic nerve and some of its branches were cut and placed on platinum wire electrodes for antidromic stimulation. Gallamine was administered to immobilize the preparation. End-expiratory CO2 level was maintained between 3 and 4 ~o. The temperature of the oil covering the cord and leg nerves was kept between 37 and 38 °C. Glass capillary microelectrodes filled with either 3 M KCI, 1 M K-acetate or 0.5 M K3-citrate were used for intracellular recording. Motoneurons considered acceptable had stable action potentials of at least 30 mV, but the majority of cells had action potentials greater than 50 mV. The pyramidal tract and nucleus ruber were stimulated by pulses of 0.1-1.0 msec duration, 1-4 times the threshold of the antidromically evoked cortical potential (i.e. 5-10 V). Peripheral nerves were stimulated by 0.1 msec pulses of supramaximal intensity. Synaptic potentials were electronically averaged (usually 32 sweeps, occasionally 64 sweeps; bin width 0.1 msec) and the time of onset of the response was determined from computer printouts. To enable comparisons between cats of various sizes, allowance had to be made for varying conduction distances. To this end, "pathway" velocities were computed by dividing the distance from the point of stimulation in the brain stem to the point of recording in the spinal cord by the latency of synaptic potentials. This pathway velocity is less than the conduction velocity in the descending tract, for the latency included time spent in traversing synapses at the segmental level. According to Illert et al. 9 and to Hongo et al. s at least two synapses are interposed between corticospinal tract and rubrospinal tract terminals and motoneurons. Antidromic conduction velocities were calculated conventionally by dividing conduction distance by latency of invasion. Fig. 1A shows the relationship of antidromic and corticospinal tract pathway velocities in 123 motoneurons. It is clear that the distribution of points in Fig. 1A is random (rank correlation, r = 0.03; probability of chance distribution P i> 0.5). Since computation of a pathway velocity may introduce error, we have compared antidromic conduction velocities and latencies of synaptic input for each experiment where more than 5 or 6 cells were encountered. An example is shown in Fig. 1B. Here, as in all other individual experiments, a correlation could not be detected between antidromic velocity and latency of input from pyramidal tract. Since, turthermore, different muscles represent different functional groups, the combining of which may confound the results, we have also considered the relationship of pyramidal input and antidromic conduction for each muscle nerve separately. When separated according to different peripheral nerves, the distribution of points was no less random than when viewed together as in Fig. 1A. Finally, when only excitatory PSPs, recorded with K3-citrate and K-acetate electrodes were considered, still no correlation between the axonal or corticospinal velocities was revealed. Rubrospinal pathway velocities were measured in 38 cells. Their relationship
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179
© Elsevier/North-HollandBiomedicalPress, Amsterdam- Printed in The Netherlands
Velocity of supraspinal input and conduction velocity of axons of spinal motoneurons
TERRY C. PELLMARand G. G. SOMJEN Department o f Physiology and Pharmacology, Duke University, Durham, N.C. 27710 (U.S.A.)
(Accepted October 14th, 1976)
Based on their observations of reflexes, Sherrington and his associatesa inferred that red muscles were involved primarily in sustained postural contractions while pale muscles were used in fast voluntary movements. Further investigation1,11,1a has shown that within mixed muscles, pale fibers contract quickly and are innervated by large motoneurons with fast axons, whereas red fibers contract more slowly and receive input from smaller, more slowly conducting motoneurons. One might expect motor units of different time characteristics to be activated in a selective manner according to the temporal requirements of the movement. If so, then large motoneurons should be accessible to faster signals from supraspinal structures than smaller motoneurons. The time taken in the conduction and transmission of impulses is, of course, of little consequence for steadily maintained contraction but may well be significant for the accurate timing of phasic movements. Time requirements of inhibition would be similar to those of excitation. A positive correlation could therefore be expected between the latency of synaptic potentials evoked by stimulation of descending pathways and the latency of antidromic invasion of motoneurons in response to stimulation of their axons. It should be emphasized that it is the total time required for a signal to travel from the b:ain to the spinal motoneuron which is important for the testing of this hypothesis and not just the conduction velocity of the descending fibers. An analogous correlation has been observed between velocities of input to and output from lateral geniculate neurons in the visual pathway7. We have recorded antidromically conducted action potentials of motoneurons in the lumbosacral spinal cord of cats and the synaptic potentials evoked by way of the corticospinal and rubrospinal tracts. Experiments were conducted on 23 animals; 19 under chloralose anesthesia (initially 40-50 mg/kg body wt., i.v.); two under Nembutal anesthesia and two unanesthetized functionally decerebrate. In 11 of the anesthetized animals, the medulla oblongata was transected sparing only the pyramidsL Forked stimulating electrodes with interpolar distance of 1 mm were inserted into the right pyramidal tract, rostral to the plane of transection. In the 10 other anesthetized animals the brain stem remained intact; similar stimulating electrodes were placed in the pyramidal tract and concentric electrodes were placed in the right nucleus ruber.
180 Placement of the pyramidal tract electrode was guided by observing the antidromic evoked potential recorded from primary motor cortex. Following each experiment, the electrode placements and the transections were histologically verified. It found unsatisfactory, data were rejected. The lumbosacral spinal cord was exposed by laminectomy. Dorsal roots on the left side of L6-SI segments were cut. The left sciatic nerve and some of its branches were cut and placed on platinum wire electrodes for antidromic stimulation. Gallamine was administered to immobilize the preparation. End-expiratory CO2 level was maintained between 3 and 4 ~o. The temperature of the oil covering the cord and leg nerves was kept between 37 and 38 °C. Glass capillary microelectrodes filled with either 3 M KCI, 1 M K-acetate or 0.5 M K3-citrate were used for intracellular recording. Motoneurons considered acceptable had stable action potentials of at least 30 mV, but the majority of cells had action potentials greater than 50 mV. The pyramidal tract and nucleus ruber were stimulated by pulses of 0.1-1.0 msec duration, 1-4 times the threshold of the antidromically evoked cortical potential (i.e. 5-10 V). Peripheral nerves were stimulated by 0.1 msec pulses of supramaximal intensity. Synaptic potentials were electronically averaged (usually 32 sweeps, occasionally 64 sweeps; bin width 0.1 msec) and the time of onset of the response was determined from computer printouts. To enable comparisons between cats of various sizes, allowance had to be made for varying conduction distances. To this end, "pathway" velocities were computed by dividing the distance from the point of stimulation in the brain stem to the point of recording in the spinal cord by the latency of synaptic potentials. This pathway velocity is less than the conduction velocity in the descending tract, for the latency included time spent in traversing synapses at the segmental level. According to Illert et al. 9 and to Hongo et al. s at least two synapses are interposed between corticospinal tract and rubrospinal tract terminals and motoneurons. Antidromic conduction velocities were calculated conventionally by dividing conduction distance by latency of invasion. Fig. 1A shows the relationship of antidromic and corticospinal tract pathway velocities in 123 motoneurons. It is clear that the distribution of points in Fig. 1A is random (rank correlation, r = 0.03; probability of chance distribution P i> 0.5). Since computation of a pathway velocity may introduce error, we have compared antidromic conduction velocities and latencies of synaptic input for each experiment where more than 5 or 6 cells were encountered. An example is shown in Fig. 1B. Here, as in all other individual experiments, a correlation could not be detected between antidromic velocity and latency of input from pyramidal tract. Since, turthermore, different muscles represent different functional groups, the combining of which may confound the results, we have also considered the relationship of pyramidal input and antidromic conduction for each muscle nerve separately. When separated according to different peripheral nerves, the distribution of points was no less random than when viewed together as in Fig. 1A. Finally, when only excitatory PSPs, recorded with K3-citrate and K-acetate electrodes were considered, still no correlation between the axonal or corticospinal velocities was revealed. Rubrospinal pathway velocities were measured in 38 cells. Their relationship
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