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Descending long-spinal excitation of lumbar alpha and gamma motoneurons evoked by stretch of dorsal neck muscles
Brain Research, 140 (1978) 165-170 © Elsevier/North-Holland Biomedical Press
165
Descending long-spinal excitation of lumbar alpha and gamma motoneurons evoked by stretch of dorsal neck muscles
K. S. K. MURTHY, P. L. GILDENBERG and J. E. MARCHAND Department of Surgery ( Neurosurgery) and Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston, Houston, Texas 77030 ( U.S. A.)
(Accepted August 24th, 1977)
Descending propriospinal effects on lumbar motoneurons have been studied mainly through electrical stimulation of the brachial plexus or of nerves to the forelimb or neck muscles1,2,15,16,2L The effects on lumbar alpha motoneurons originating from the dorsal muscles of the neck have been shown to be a facilitation of the monosynaptic and polysynaptic segmental reflexes 1. Long-spinal reflexes elicited by electrical stimulation of cutaneous and muscle nerves in the hind limb have been shown to be augmented by a conditioning stimulus to the nerve innervating the biventer cervicis muscle 1 and by natural stimulation of the dorsal neck muscle proprioceptors 22. The coactivation of alpha and gamma motor systems innervating the ankle extensor muscle soleus has also been demonstrated on ventroflexion of the neck in the decerebrate cat v. Evidence is presented here that such coactivation of alpha and gamma motoneurons in a propriospinal reflex may employ a recruitment of the gamma and alpha motoneurons in the order of their sizes. The results described here are from a study of the lumbar gamma motoneurons in the cat under light sodium pentobarbital anesthesia. Adult cats were anesthetized with an initial intraperitoneal dose of 30 mg/kg sodium pentobarbital which was supplemented by smaller intravenous doses (2 mg/kg) at approximately 90-rain intervals to maintain a low level of anesthesia. A dissection of the left hind limb was performed to permit electrical stimulation of the peripheral nerves (muscle and cutaneous) and for the application of stretch to the triceps surae muscles. A lumbar laminectomy L4-Sa levels) was carried out and efferent unit activity recorded from ventral root filaments. The level of anesthesia was such that an excitation in the form of a pinna twist or pinching of the foot caused a generalized movement of the limbs or shaking of the head 11. The ventral root (LT) filament from which recording was made was in some cases cut distally to facilitate recording, but all the other ventral roots as well as dorsal roots were left intact, preserving synaptic activation of the motoneurons. G a m m a motoneurons were normally identified by their spontaneous activity in the absence of any stimulus and confirmed by measurement of conduction velocity obtained through a recording of the conduction time between two recording electrodes placed on the same filament with a spacing of 5-10 mm. Alpha motor units,
166
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Fig. 1. lnterspike interval histograms of a semitendinosus gamma motoneuron showing: sFontar.eous background activity (a) and effects of ipsilateral ankle extension (b) and eontralateral ankle extension (c). Maximum excitation occurred through a propriospinal reflex on stretch applied to ccntralateral dorsal neck muscles - - occipitoscapularis (d) and splenius (f), which are long-lasting as demonstrated by the histogram in (e) which was obtained two minutes after release of the stretch applied to the occipitoscapularis as in (d). Each interval histogram consists of 1000 successive intervals obtained in approximately two-minute periods of observation. The mean intervals are marked to the right of each curve, abscissa in intervals. Vertical calibration denotes numl;er of intervals in each bin. Total sweep for each trace corresponds to 256 bins. when encountered in the same rootlet could be clearly distinguished by their larger sizes~,2L The ventral root unit activity was processed t h r o u g h suitable amplifiers and printed on a light-sensitive paper recorder (TECA. TE-4 electromyograph). Simultaneous analysis o f the statistical parameters was performed t h r o u g h a c o m p u t a t i o n of interspike interval histograms using a Nicolet 1072 computer. The results described here are from 5 experiments. Fig. 1 illustrates the interval histograms for a semitendinosus fusimotor neuron which received excitation showing crossed effects from the hind limb (Fig. lc) and from the contralateral dorsal neck muscles, splenius and occipitoscapularis (Fig. ld and f). These propriospinal excitatory effects are long-tasting, as can be deduced f r o m the histogram of Fig. l e, which was obtained two minutes after releasing the stretch o f the contralate ral occipitoscapularis muscle. The ventral rootlet was not cut during the above recordings which permitted the identification of the muscle innervated by this g a m m a unit. Similar effects were observed in another experiment in which the ventral rootlet had two g a m m a units and two alpha units. All the units had been initially silent but became active when the contralateral dorsal neck muscles were stretched (Fig. 2) with
167
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Fig. 2. Lumbar alpha (a~, az) and gamma (g~, g~) units recruited by stretch applied to contralateral dorsal neck muscle (occipitoscapularis). Records are continuous from left to right and top to bottom. The breaks in lines 2 and 4 are about one second each. The coactivated alpha units are 'tonic' type with a steady rate of firing. Recruitment is observed even between the two gamma units.
the gamma motoneurons being recruited first. Recruitment occurred in the order of the sizes of the spikes, even of the two gamma motoneurons in the filament. By progressively increasing the amount of stretch applied to the contralateral occipitoscapularis, two alpha units were also recruited, the first unit firing tonically. The recruitment order of gamma and alpha units was found to be preserved even when different modes of excitation converged on the same units. These were (1) pinna twist; (2) pinching of the ipsilateral hind paw; (3) stretch of the ipsilateral triceps surae muscles by a pull on the Achille's tendon (Fig. 3); (4) electrical stimulation of the nerve to the medial gastrocnemius muscle; or (5) flexion of the contralateral forelimb. Although the recruitment order of gamma units followed by alpha units was preserved in all the tests employing natural stimuli, electrical stimulation of the medial gastrocnemius muscle nerve at progressively increasing strength caused the larger alpha unit to be recruited earlier at a lower stimulus strength than that which excited the smaller alpha unit. Also, the smaller of the two gamma units observed in Fig. 2 on stretch of occipitoscapularis does not appear in the records of Fig. 3 taken during a stretch applied to the triceps surae, presumably due to the stronger activation through the propriospinal pathway than the proprioceptive activation from the same limb. This was observed again when flexion of the contralateral forelimb elicited activity in gamma units which had not been spontaneously active prior to the test.
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Fig. 3. Recruitment of gamma (g) and alpha (al, a2) motor units (same as in Fig, 2) recorded from the ventral root filament in response to a stretch of the triceps surae muscles by ankle flexion. The muscle tendons had not been cut. A shows orderly recruitment (top to bottom) as tke muscles are progressively stretched; in B the muscles are released from stretch. The garnma unit is the last to drop out. The gamma unit in this record is g~, observed in Fig. 2; gl is not activated by this test.
The destinations of the gamma and alpha units recorded in this experiment (Figs. 2 and 3) are not known since the ventral root filament had been cut distally. The alpha units most likely innervated the synergists of the ankle extensors (Fig. 3), since they were excited by stretch of the triceps surae muscles. It is, however, debatable whether the g a m m a motor units observed in the above case of recruitment would innervate the same group of muscles. Autogenetic excitatory reflex effects o n gamma motoneurons have so far been demonstrated under extreme conditions of excitability as observed in the decerebrate animal on application of a vibratory stimulus to the muscles innervated by themX0, 24, possibly through activation of polysynaptic supra-
169 spinal pathways involved in a tonic reflex8. Under conditions of pentobarbital anesthesia similar to the present experiments, Proske and Lewis 2° were able to detect only very weak autogenetic excitatory effects on gamma motoneurons. On the other hand, medial gastrocnemius gamma motoneurons have been shown to be excited by neck flexion x2 under light pentobarbital anesthesia, an identical stimulus to that illustrated in Fig. 2. Also, alpha-gamma coactivation has been demonstrated in the soleus of the decerebrate cat on neck ventroflexion by Eldred et al. v, even though they recorded gamma effects indirectly through effects on muscle spindle discharge. In the present study, similar long-spinal effects have been observed in other experiments where the gamma motoneurons were found to innervate the biarticular muscles of the thigh, posterior biceps and semitendinosus (Fig. 1). An alternative possibility is that the coactivation of alpha and gamma motoneurons observed in this study is another example of the classical alpha-gamma linkage that has been seen in a number of cases 13, both the alpha and gamma motoneurons innervating the semitendinosus, which is a biarticular bifunctional muscle. Though it is classified as a physiological flexor since it participates in the flexion reflex6 and functions as a knee flexor, the semitendinosus also functions as an extensor of the hip joint 9. Such dual behavior of the semitendinosus motoneurons has been demonstrated by the dual burst of electromyographic activity during locomotion 19. Perret 18 found that, for such locomotory rhythms, coactivation of fusimotor neurons occurred during extensor phase of the EMG. In the present study, it was probably such a coactivation of alpha and gamma motoneurons that has been observed. Although many factors may be involved in deciding the recruitment order of motor units, the most important consideration is perhaps the amount of synaptic activation of motoneuronsa, 4 and the state of the interneurons, which process a variety of segmental, intersegmental and supraspinal inputs prior to activation of the motoneurons14, 23. Several significant features relating to the recruitment of gamma and alpha motoneurons were observed: (1) The gamma units that were found to be recruited were slow-riring and highly irregular in discharge rates and appeared to be most depressed by barbiturate anesthesia; and (2) The alpha units that were easily recruited with the gamma units were the tonically firing, highly regular units. The phasic units became active only at high stimulus intensities. The propriospinal link demonstrated here involving the neck muscle proprioceptors and lumbar gamma and alpha motoneurons must be a strong one to occur with a weak stretch applied to a single muscle (Fig. 2). Effects due to possible activation of the muscle spindles in the neighboring splenius muscle 21 or of the stretch receptors in the vertebral joints iv cannot be entirely ruled out since the occipitoscapularis muscle was not completely freed of connective tissue when the stretch was applied to its rostral tendon. Such an influence would, however, be reinforcing (Fig. 1).
170
This study was funded by a General Research Support Grant (5 S01-RR-0474503) from The University of Texas Medical School at Houston.
1 Abrahams, V. C., Neck muscle proprioceptors and a role of the cerebral cortex in postural reflexes in subprimates, Rev. Canad. Biol., 31 (1972) 115-130. 2 Abrahams, V. C. and Falchetto, S., Hind leg ataxia of cervical origin and cervico-lumbar spinal interactions with a supratentorial pathway, J. Physiol. (Lond.), 203 (1969) 435-447. 3 Burke, R. E., On the central nervous system control of fast and slow twitch motor units. In J. E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. IlI, Karger, Basel, pp. 69-94. 4 Burke, R. E. and Edgerton, V. R., Motor unit properties and selective involvement in movement. In J. H. Wilmore and J. F. Keogh (Eds.), Exercise and Sports Science Reviews, VoL 3, Academic Press, New York, 1975, pp. 31-81. 5 Clamann, H. P. and Henneman, E., Electrical measurement of axon diameter and its use in relating motoneuron size to critical firing level, J. Neurophysiol., 39 (1976) 844-851. 6 Eccles, R. M. and Lundberg, A., Synaptic actions in motoneurone by afferents which may evoke the flexion reflex, Arch. ital. Biol., 97 (1959) 199-221. 7 Eldred, E., Granit, R. and Merton, P. A., Supraspinal control of the muscle spindles and its significance, J. Physiol. (Lond.), 122 (1953) 498-523. 8 EIlaway, P. H., Pascoe, J. E. and Trott, J. R., The effect upon fusimotor neurones of small, brief stretches of their muscles, J. Physiol. (Lond.), 258 (1976) 48P~,9P. 9 Engberg, I. and Lundberg, A., An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion, Acta physiol, scand., 75 (1969) 614-630. 10 Fromm, C. and Noth, J., Reflex responses of gamma motoneurones to vibration of the muscle they innervate, J. Physiol. (Lond.), 256 (1976) 117-136. I 1 Gilman, S., Patterns of motoneurone responses to natural stimuli. In T. Desiraju (Ed.), Mechanisms in Transmission of Signals for Conscious Behavior, Elsevier, Holland, 1976. 12 Gilman, S. and Ebel, H. C., Fusimotor neuron responses to natural stimuli as a function of prestimulus fusimotor activity in decerebellate cats, Brain Research, 21 (1970) 367-384. 13 Granit, R., The Basis of Motor Control, Academic Press, New York, 1970. 14 Henneman, E., Somjen, G. and Carpenter, D. O., Excitability and inhibitability of motoneurons of different sizes, J. Neurophysiol., 28 (1965) 59%620. 15 Lloyd, D. P. C., Mediation of descending long spinal reflex activity, J. Neurophysiol., 5 (1942) 435-458. 16 Lloyd, D. P. C. and Mclntyre, A. K., Analysis of forelimb-hindlimb reflex activity in acutely decapitate cats, J. Neurophysiol., 11 (1948) 455-470. 17 McCouch, G. P., Deering, I. D. and Ling, T. H., Location of receptors for tonic neck reflexes, J. Neurophysiol., 14 (1951) 191-195. 18 Perret, C., Activit6s eff6renter et g6n6rateur de rythme locomoteur chez le chat, J. Ph3sioL (Paris), 69 (1974) 284A. 19 Perret, C. and Cabelguen, J., Central and reflex participationin the timing of locomotor activations of a bifunctional muscle, the semitendinosus in the cat, Brain Research, 106 (1976) 390-395. 20 Proske, U. and Lewis, D. M., The effects of muscle stretch and vibration on fusimotor activity in tee lightly anesthetized cat, Brain Research, 46 (1972) 55-70. 21 Richmond, F. J. R. and Abrahams, V. C., Morphology and distribution ofspindles in dorsal muscles of the cat neck, J. Neurophysiol., 38 (1975) 1322-1339. 22 Shimamura, M. and Akert, K., Peripheral nervous relations of propriospinal and spino-bulbospinal reflex systems, .lap. J. PhysioL, 15 (1965) 638-647. 23 Somjen, G., Carpenter, D. O. and Henneman, E., Responses of motoneurones of different sizes to graded stimulation of supraspinal centers of the brain, J. Neurophysiol., 28 (1965) 958--965. 24 Trott, J. R., The effect of low amplitude muscle vibration on the discharge of fusimotor neurones in the decerebrate cat., J. Physiol. (Lond.), 255 (1976) 635-649. 25 Van der Meulen, J. P., Differentiation of alpha and gamma motor unit discharge in muscle nerves. In S. Locke (Ed.), Modern Neurology, Little, Brown, Boston, 1969, pp. 121-134.
165
Descending long-spinal excitation of lumbar alpha and gamma motoneurons evoked by stretch of dorsal neck muscles
K. S. K. MURTHY, P. L. GILDENBERG and J. E. MARCHAND Department of Surgery ( Neurosurgery) and Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston, Houston, Texas 77030 ( U.S. A.)
(Accepted August 24th, 1977)
Descending propriospinal effects on lumbar motoneurons have been studied mainly through electrical stimulation of the brachial plexus or of nerves to the forelimb or neck muscles1,2,15,16,2L The effects on lumbar alpha motoneurons originating from the dorsal muscles of the neck have been shown to be a facilitation of the monosynaptic and polysynaptic segmental reflexes 1. Long-spinal reflexes elicited by electrical stimulation of cutaneous and muscle nerves in the hind limb have been shown to be augmented by a conditioning stimulus to the nerve innervating the biventer cervicis muscle 1 and by natural stimulation of the dorsal neck muscle proprioceptors 22. The coactivation of alpha and gamma motor systems innervating the ankle extensor muscle soleus has also been demonstrated on ventroflexion of the neck in the decerebrate cat v. Evidence is presented here that such coactivation of alpha and gamma motoneurons in a propriospinal reflex may employ a recruitment of the gamma and alpha motoneurons in the order of their sizes. The results described here are from a study of the lumbar gamma motoneurons in the cat under light sodium pentobarbital anesthesia. Adult cats were anesthetized with an initial intraperitoneal dose of 30 mg/kg sodium pentobarbital which was supplemented by smaller intravenous doses (2 mg/kg) at approximately 90-rain intervals to maintain a low level of anesthesia. A dissection of the left hind limb was performed to permit electrical stimulation of the peripheral nerves (muscle and cutaneous) and for the application of stretch to the triceps surae muscles. A lumbar laminectomy L4-Sa levels) was carried out and efferent unit activity recorded from ventral root filaments. The level of anesthesia was such that an excitation in the form of a pinna twist or pinching of the foot caused a generalized movement of the limbs or shaking of the head 11. The ventral root (LT) filament from which recording was made was in some cases cut distally to facilitate recording, but all the other ventral roots as well as dorsal roots were left intact, preserving synaptic activation of the motoneurons. G a m m a motoneurons were normally identified by their spontaneous activity in the absence of any stimulus and confirmed by measurement of conduction velocity obtained through a recording of the conduction time between two recording electrodes placed on the same filament with a spacing of 5-10 mm. Alpha motor units,
166
41
I2° ()
5'0
1()0
msec
oJ"
50
100
Fig. 1. lnterspike interval histograms of a semitendinosus gamma motoneuron showing: sFontar.eous background activity (a) and effects of ipsilateral ankle extension (b) and eontralateral ankle extension (c). Maximum excitation occurred through a propriospinal reflex on stretch applied to ccntralateral dorsal neck muscles - - occipitoscapularis (d) and splenius (f), which are long-lasting as demonstrated by the histogram in (e) which was obtained two minutes after release of the stretch applied to the occipitoscapularis as in (d). Each interval histogram consists of 1000 successive intervals obtained in approximately two-minute periods of observation. The mean intervals are marked to the right of each curve, abscissa in intervals. Vertical calibration denotes numl;er of intervals in each bin. Total sweep for each trace corresponds to 256 bins. when encountered in the same rootlet could be clearly distinguished by their larger sizes~,2L The ventral root unit activity was processed t h r o u g h suitable amplifiers and printed on a light-sensitive paper recorder (TECA. TE-4 electromyograph). Simultaneous analysis o f the statistical parameters was performed t h r o u g h a c o m p u t a t i o n of interspike interval histograms using a Nicolet 1072 computer. The results described here are from 5 experiments. Fig. 1 illustrates the interval histograms for a semitendinosus fusimotor neuron which received excitation showing crossed effects from the hind limb (Fig. lc) and from the contralateral dorsal neck muscles, splenius and occipitoscapularis (Fig. ld and f). These propriospinal excitatory effects are long-tasting, as can be deduced f r o m the histogram of Fig. l e, which was obtained two minutes after releasing the stretch o f the contralate ral occipitoscapularis muscle. The ventral rootlet was not cut during the above recordings which permitted the identification of the muscle innervated by this g a m m a unit. Similar effects were observed in another experiment in which the ventral rootlet had two g a m m a units and two alpha units. All the units had been initially silent but became active when the contralateral dorsal neck muscles were stretched (Fig. 2) with
167
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Fig. 2. Lumbar alpha (a~, az) and gamma (g~, g~) units recruited by stretch applied to contralateral dorsal neck muscle (occipitoscapularis). Records are continuous from left to right and top to bottom. The breaks in lines 2 and 4 are about one second each. The coactivated alpha units are 'tonic' type with a steady rate of firing. Recruitment is observed even between the two gamma units.
the gamma motoneurons being recruited first. Recruitment occurred in the order of the sizes of the spikes, even of the two gamma motoneurons in the filament. By progressively increasing the amount of stretch applied to the contralateral occipitoscapularis, two alpha units were also recruited, the first unit firing tonically. The recruitment order of gamma and alpha units was found to be preserved even when different modes of excitation converged on the same units. These were (1) pinna twist; (2) pinching of the ipsilateral hind paw; (3) stretch of the ipsilateral triceps surae muscles by a pull on the Achille's tendon (Fig. 3); (4) electrical stimulation of the nerve to the medial gastrocnemius muscle; or (5) flexion of the contralateral forelimb. Although the recruitment order of gamma units followed by alpha units was preserved in all the tests employing natural stimuli, electrical stimulation of the medial gastrocnemius muscle nerve at progressively increasing strength caused the larger alpha unit to be recruited earlier at a lower stimulus strength than that which excited the smaller alpha unit. Also, the smaller of the two gamma units observed in Fig. 2 on stretch of occipitoscapularis does not appear in the records of Fig. 3 taken during a stretch applied to the triceps surae, presumably due to the stronger activation through the propriospinal pathway than the proprioceptive activation from the same limb. This was observed again when flexion of the contralateral forelimb elicited activity in gamma units which had not been spontaneously active prior to the test.
168
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Fig. 3. Recruitment of gamma (g) and alpha (al, a2) motor units (same as in Fig, 2) recorded from the ventral root filament in response to a stretch of the triceps surae muscles by ankle flexion. The muscle tendons had not been cut. A shows orderly recruitment (top to bottom) as tke muscles are progressively stretched; in B the muscles are released from stretch. The garnma unit is the last to drop out. The gamma unit in this record is g~, observed in Fig. 2; gl is not activated by this test.
The destinations of the gamma and alpha units recorded in this experiment (Figs. 2 and 3) are not known since the ventral root filament had been cut distally. The alpha units most likely innervated the synergists of the ankle extensors (Fig. 3), since they were excited by stretch of the triceps surae muscles. It is, however, debatable whether the g a m m a motor units observed in the above case of recruitment would innervate the same group of muscles. Autogenetic excitatory reflex effects o n gamma motoneurons have so far been demonstrated under extreme conditions of excitability as observed in the decerebrate animal on application of a vibratory stimulus to the muscles innervated by themX0, 24, possibly through activation of polysynaptic supra-
169 spinal pathways involved in a tonic reflex8. Under conditions of pentobarbital anesthesia similar to the present experiments, Proske and Lewis 2° were able to detect only very weak autogenetic excitatory effects on gamma motoneurons. On the other hand, medial gastrocnemius gamma motoneurons have been shown to be excited by neck flexion x2 under light pentobarbital anesthesia, an identical stimulus to that illustrated in Fig. 2. Also, alpha-gamma coactivation has been demonstrated in the soleus of the decerebrate cat on neck ventroflexion by Eldred et al. v, even though they recorded gamma effects indirectly through effects on muscle spindle discharge. In the present study, similar long-spinal effects have been observed in other experiments where the gamma motoneurons were found to innervate the biarticular muscles of the thigh, posterior biceps and semitendinosus (Fig. 1). An alternative possibility is that the coactivation of alpha and gamma motoneurons observed in this study is another example of the classical alpha-gamma linkage that has been seen in a number of cases 13, both the alpha and gamma motoneurons innervating the semitendinosus, which is a biarticular bifunctional muscle. Though it is classified as a physiological flexor since it participates in the flexion reflex6 and functions as a knee flexor, the semitendinosus also functions as an extensor of the hip joint 9. Such dual behavior of the semitendinosus motoneurons has been demonstrated by the dual burst of electromyographic activity during locomotion 19. Perret 18 found that, for such locomotory rhythms, coactivation of fusimotor neurons occurred during extensor phase of the EMG. In the present study, it was probably such a coactivation of alpha and gamma motoneurons that has been observed. Although many factors may be involved in deciding the recruitment order of motor units, the most important consideration is perhaps the amount of synaptic activation of motoneuronsa, 4 and the state of the interneurons, which process a variety of segmental, intersegmental and supraspinal inputs prior to activation of the motoneurons14, 23. Several significant features relating to the recruitment of gamma and alpha motoneurons were observed: (1) The gamma units that were found to be recruited were slow-riring and highly irregular in discharge rates and appeared to be most depressed by barbiturate anesthesia; and (2) The alpha units that were easily recruited with the gamma units were the tonically firing, highly regular units. The phasic units became active only at high stimulus intensities. The propriospinal link demonstrated here involving the neck muscle proprioceptors and lumbar gamma and alpha motoneurons must be a strong one to occur with a weak stretch applied to a single muscle (Fig. 2). Effects due to possible activation of the muscle spindles in the neighboring splenius muscle 21 or of the stretch receptors in the vertebral joints iv cannot be entirely ruled out since the occipitoscapularis muscle was not completely freed of connective tissue when the stretch was applied to its rostral tendon. Such an influence would, however, be reinforcing (Fig. 1).
170
This study was funded by a General Research Support Grant (5 S01-RR-0474503) from The University of Texas Medical School at Houston.
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