Acta physiol. scand. 1975. 94. 130-132 From the Department of Physiology, University of Goteborg, Sweden
a-7-Linkage in the Spinal Generator for Locomotion in the Cat BY A. SJOSTROM and P. ZANGGER
Grillner and Zangger (1974) reported that after a complete transection of all dorsal roots, preparations spinalized at lower thoracic or upper lumbar levels can still produce rhythmic locomotor like activity with an alternate activation of flexors and extensors, provided that they have been injected with DOPA, DOPA and Nialamide, Clonidine i.v. or that the transection of the spinal cord is chronic. The present study was undertaken to see whether or not y-motoneurones to the appropriate muscles are coactivated with the a-motoneurones during this rhythmic activity. The y-motoneurone activity has been recorded in the form of single y-efferents isolated in peripheral nerve filaments and identified by their conduction velocity from the ventral roots (see Bergmans and Grillner 1969) to either a flexor (tenuissimus) or an extensor (lateral gastrocnemius). Also muscle spindle afferents (primary endings), identified conventionally (cf. Matthews 1972), were recorded from a flexor (anterior tibial) and an extensor (soleus). The preparations were decerebrated and spinal (Th 12 to 13) without anesthesia from 2 h prior to the beginning of the recording period. All dorsal roots were transected, and 50 mg/kg Nialamide was injected i.v. followed by up to 50 mg/kg DOPA. After this injection spontaneous rhythmic activity (0.5-1.2 Hz) could occur, but during uni- or bilateral continuous stimulation (10-200 Hz) of the cut dorsal roots (L 5 or L 6), the rhythmic efferent activity increased in frequency and became more regular. When recording y-efferents the preparations were curarized and a- and y-motoneurones were recorded in filaments; when recording primary endings a strain gauge was connected to the muscle under investigation. The length of the muscle was meascred in relation to the maximal length and the corresponding joint angle (Grillner and Udo 1971). Fig. 1 A shows the discharge in a primary ending from a soleus spindle and the marked acceleration during each period of extrafusal contraction. For comparison (B) is shown the typical unloading of the ending occuring when the nerve is stimulated with a single shock. The graph in D shows the rhythmic increase in discharge frequency in a single extensor y-motoneuron. The bars below show that the periods during which the a-motoneurones are accelerated coincide with the increased y-activity. Therefore it is no doubt that the results shown in A is due to a-y-coactivation. In C is shown that a- and y-motoneurones to a flexor muscle are also coactivated. 130
131
a-7-LINKAGE IN STEPPING
+ 15N* B
A
sol. prim. ending
IS
HZ
C
7-ten.
.
. . ...
... . . ..
_..._.
0
5
- a-ten. - TA -
S
0
- a-LG -
-T A -
5
s
- - - - -
Fig. 1. Rhythmic a-y-coactivation to flexors and extensors. A shows the activity of a single primary (conduction velocity 85 m/s) ending from an ankle extensor (m. soleus) recorded in a dorsal root filament L 7 (upper trace) during rhythmic isometric contraction of the muscle (tension, lower trace). The muscle was held at a length corresponding to 60" ankle flexion, resulting in a resting discharge of 36 Hz. Continuous bilateral stimulation of L 6 dorsal roots (100 Hz, 60 p A squarewave pulses of 0.2 ms duration). In B is shown a twitch contraction after stimulation of the muscle nerve obtained just before the recordings in A. C shows the frequency of discharge (ordinate) in a single flexor y-efferent (conduction velocity 35 m/s) during spinal stepping recorded from a tenuissimus nerve filament. The recorded sequence was taken just after termination of a period of ipsilateral continuous stimulation of the dorsal root L 6. Dots mark the instantaneous frequency (l/interval length); the curve is plotted with a floating average over the 8 nearest intervals. The horizontal bars below the graph indicate the duration of the activity of a single a-efferent recorded in the same filament (a-ten.) and the activity in a nerve to an ankle flexor (TA, tibialis anterior). The resolution for the frequency plot was limited by the input device to the computer (digitizer table). D shows rhythmic discharges of a single extensor y-efferent (conduction velocity 29 m/s) recorded in a lateral gastrocnemius (LG) nerve filament during ipsilateral stimulation of L 5 dorsal root (100 Hz, 30pA). Presentation as in C . The bars indicate the period of activity in a single a-efferent recorded in the same nerve filament (a-LG). Note time and tension (100 g.wt. equals 0.981 N) calibration for A and B.
Hence it can be concluded that the central spinal mechanism that gpnerates this rhythmic locomotor activity in fact is coactivating a- and y-motoneurones, i.e. there is a central spinal a-y-linkage. This is in agreement with the predictions made from the studies of a-;j-linkage in the late discharges occuring after DOPA (Grillner 1969, see also Perret 1973). The entire pattern of muscle activity in locomotion can be generated in the low spinal animal (Grillner 1973) and it thus appears that these movements are a-y-linked, and it follows that the findings of a-y-coactivation in high decerebrate walking cats should also be due to a spinal mechanism (Severin et al. 1967). The helpful discussions with, and the valuable criticism from Dr. Sten Grillner is greatfully acknowledged.
132
A. SJOSTROMAND P. ZANGGER
This work was supported by a grant from the Swedish Medical Research Council (14X-3026) and a grant from the Medical Faculty in Goteborg. P. Zangger was supported by the Swiss National Foundation. The skilful assistance of Mrs. M. Svanberg is gratefully acknowledged.
References BERCMANS, J. and S. GRILLNER, Reciprocal control of spontaneous activity and reflex effects in static and dynamic y-motoneurones revealed by an injection of DOPA. Acta physiol. scand. 1969. 77. 106-124. GRILLNER, S., Supraspinal and segmental control of static and dynamic y-motoneurones in the cat. Acta physiol. scand. 1969. Suppl. 327. 1-34. GRILLNER, S., Locomotion in the spinal cat. In “Control of Posture and Locornofion”. Eds. R. B. Stein et al. Plenum Press, New York 1973. 515-535. GRILLNER,S. and M. UDO,Motor unit activity and stiffness of the contracting muscle fibres in the tonic stretch reflex. Acfa physiol. scand. 1971. 81. 4 2 2 4 2 4 . GRILLNER, S. and P. ZANGGER, Locomotor movements generated by the deafferented spinal cord. Acta physiol. scand. 1974. 91. 38-39 A. MATTHEWS, P. B. C., Mammalian muscle recepfors and their central acrions. Edward Arnold (Publ.) Ltd. London 1972. PERRET,C., Analyse des mkchanismes d’une activitk de type locomoteur chez le chat. Thise de doct. Paris 1973. SEVERIN, F. V., G. N. ORLOVSKY and M. L. SHIK,Work of the muscle receptors during controlled locomotion. Biofizika 1967. 12. 575-586. (Eng. transl.)
a-7-Linkage in the Spinal Generator for Locomotion in the Cat BY A. SJOSTROM and P. ZANGGER
Grillner and Zangger (1974) reported that after a complete transection of all dorsal roots, preparations spinalized at lower thoracic or upper lumbar levels can still produce rhythmic locomotor like activity with an alternate activation of flexors and extensors, provided that they have been injected with DOPA, DOPA and Nialamide, Clonidine i.v. or that the transection of the spinal cord is chronic. The present study was undertaken to see whether or not y-motoneurones to the appropriate muscles are coactivated with the a-motoneurones during this rhythmic activity. The y-motoneurone activity has been recorded in the form of single y-efferents isolated in peripheral nerve filaments and identified by their conduction velocity from the ventral roots (see Bergmans and Grillner 1969) to either a flexor (tenuissimus) or an extensor (lateral gastrocnemius). Also muscle spindle afferents (primary endings), identified conventionally (cf. Matthews 1972), were recorded from a flexor (anterior tibial) and an extensor (soleus). The preparations were decerebrated and spinal (Th 12 to 13) without anesthesia from 2 h prior to the beginning of the recording period. All dorsal roots were transected, and 50 mg/kg Nialamide was injected i.v. followed by up to 50 mg/kg DOPA. After this injection spontaneous rhythmic activity (0.5-1.2 Hz) could occur, but during uni- or bilateral continuous stimulation (10-200 Hz) of the cut dorsal roots (L 5 or L 6), the rhythmic efferent activity increased in frequency and became more regular. When recording y-efferents the preparations were curarized and a- and y-motoneurones were recorded in filaments; when recording primary endings a strain gauge was connected to the muscle under investigation. The length of the muscle was meascred in relation to the maximal length and the corresponding joint angle (Grillner and Udo 1971). Fig. 1 A shows the discharge in a primary ending from a soleus spindle and the marked acceleration during each period of extrafusal contraction. For comparison (B) is shown the typical unloading of the ending occuring when the nerve is stimulated with a single shock. The graph in D shows the rhythmic increase in discharge frequency in a single extensor y-motoneuron. The bars below show that the periods during which the a-motoneurones are accelerated coincide with the increased y-activity. Therefore it is no doubt that the results shown in A is due to a-y-coactivation. In C is shown that a- and y-motoneurones to a flexor muscle are also coactivated. 130
131
a-7-LINKAGE IN STEPPING
+ 15N* B
A
sol. prim. ending
IS
HZ
C
7-ten.
.
. . ...
... . . ..
_..._.
0
5
- a-ten. - TA -
S
0
- a-LG -
-T A -
5
s
- - - - -
Fig. 1. Rhythmic a-y-coactivation to flexors and extensors. A shows the activity of a single primary (conduction velocity 85 m/s) ending from an ankle extensor (m. soleus) recorded in a dorsal root filament L 7 (upper trace) during rhythmic isometric contraction of the muscle (tension, lower trace). The muscle was held at a length corresponding to 60" ankle flexion, resulting in a resting discharge of 36 Hz. Continuous bilateral stimulation of L 6 dorsal roots (100 Hz, 60 p A squarewave pulses of 0.2 ms duration). In B is shown a twitch contraction after stimulation of the muscle nerve obtained just before the recordings in A. C shows the frequency of discharge (ordinate) in a single flexor y-efferent (conduction velocity 35 m/s) during spinal stepping recorded from a tenuissimus nerve filament. The recorded sequence was taken just after termination of a period of ipsilateral continuous stimulation of the dorsal root L 6. Dots mark the instantaneous frequency (l/interval length); the curve is plotted with a floating average over the 8 nearest intervals. The horizontal bars below the graph indicate the duration of the activity of a single a-efferent recorded in the same filament (a-ten.) and the activity in a nerve to an ankle flexor (TA, tibialis anterior). The resolution for the frequency plot was limited by the input device to the computer (digitizer table). D shows rhythmic discharges of a single extensor y-efferent (conduction velocity 29 m/s) recorded in a lateral gastrocnemius (LG) nerve filament during ipsilateral stimulation of L 5 dorsal root (100 Hz, 30pA). Presentation as in C . The bars indicate the period of activity in a single a-efferent recorded in the same nerve filament (a-LG). Note time and tension (100 g.wt. equals 0.981 N) calibration for A and B.
Hence it can be concluded that the central spinal mechanism that gpnerates this rhythmic locomotor activity in fact is coactivating a- and y-motoneurones, i.e. there is a central spinal a-y-linkage. This is in agreement with the predictions made from the studies of a-;j-linkage in the late discharges occuring after DOPA (Grillner 1969, see also Perret 1973). The entire pattern of muscle activity in locomotion can be generated in the low spinal animal (Grillner 1973) and it thus appears that these movements are a-y-linked, and it follows that the findings of a-y-coactivation in high decerebrate walking cats should also be due to a spinal mechanism (Severin et al. 1967). The helpful discussions with, and the valuable criticism from Dr. Sten Grillner is greatfully acknowledged.
132
A. SJOSTROMAND P. ZANGGER
This work was supported by a grant from the Swedish Medical Research Council (14X-3026) and a grant from the Medical Faculty in Goteborg. P. Zangger was supported by the Swiss National Foundation. The skilful assistance of Mrs. M. Svanberg is gratefully acknowledged.
References BERCMANS, J. and S. GRILLNER, Reciprocal control of spontaneous activity and reflex effects in static and dynamic y-motoneurones revealed by an injection of DOPA. Acta physiol. scand. 1969. 77. 106-124. GRILLNER, S., Supraspinal and segmental control of static and dynamic y-motoneurones in the cat. Acta physiol. scand. 1969. Suppl. 327. 1-34. GRILLNER, S., Locomotion in the spinal cat. In “Control of Posture and Locornofion”. Eds. R. B. Stein et al. Plenum Press, New York 1973. 515-535. GRILLNER,S. and M. UDO,Motor unit activity and stiffness of the contracting muscle fibres in the tonic stretch reflex. Acfa physiol. scand. 1971. 81. 4 2 2 4 2 4 . GRILLNER, S. and P. ZANGGER, Locomotor movements generated by the deafferented spinal cord. Acta physiol. scand. 1974. 91. 38-39 A. MATTHEWS, P. B. C., Mammalian muscle recepfors and their central acrions. Edward Arnold (Publ.) Ltd. London 1972. PERRET,C., Analyse des mkchanismes d’une activitk de type locomoteur chez le chat. Thise de doct. Paris 1973. SEVERIN, F. V., G. N. ORLOVSKY and M. L. SHIK,Work of the muscle receptors during controlled locomotion. Biofizika 1967. 12. 575-586. (Eng. transl.)
