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Lack of recurrent depression from motor axon collaterals of la IPSPs in dorsal spinocerebellar tract neurones
158
Braht Re~earch, 129 (1977) 158 - I (~| ~: Elsevier/North-Holland Biomedical Press
Lack of recurrent depression from motor axon collaterals of la IPSPs in dorsal spinocerebellar tract neurones
SIVERT LINDSTROM and M1TSURU TAKATA*
Department of Physiology, University qf Giiteborg, GiJteborg (Sweden) (Accepted March 3rd, 1977)
Muscle spindle la afferents have disynaptic inhibitory connexions to several spinal neurones including motoneurones 2 and the cells of origin of the ventral (VSCT) 3 and dorsal (DSCT) 4 spinocerebellar tracts. In motoneurones ° and some VSCT cellsS, 8, the Ia IPSPs can be depressed by impulses in recurrent motor axon collaterals, indicating that the same la inhibitory interneurones project to both types of cells 5,7. Disynaptic Ia IPSPs in DSCT neurones have now been conditioned by a nerve volley in the ventral roots to determine whether the same group of ia interneurones terminate also on DSCT cells. The experiments were done on 6 cats anaesthetized with a-chloralose t50-60 mg/kg). Only preparations with a good threshold separation between la and lb afferents in the nerves from thigh muscles were used 1. lntracellular recordings were obtained from DSCT neurones in Clarke's column on the left side at the level of L3-L4. Most cells were identified as belonging to the DSCT by their location, and afferent input from muscle nerves and by antidromic activation from the ipsilateral dorsolateral funiculus at the level of Th 124. Some of the cells were identified by antidromic activation from the ipsilateral anterior lobe of cerebellum using unipolar cathodal surface stimulation with constant cm rent pulses with a duration of 0.2 msec and an intensity of less than 2 mA 11. In these latter experiments the dorsal funiculi and the right spinal half were transected at the level of Th t 2. Several muscle nerves to the left hindlimb (cf. ref. 5) and the left ventral roots L5-SI were transected and their proximal ends mounted for electrical stimulation. The incoming nerve volleys were recorded triphasically from the dorsal root entry zone in the caudal L6 segment. Microelectrodes filled with 2 M potassium cttrate and with tip diameter of 1.5-2.0 #m and resistance of 3-6 M ~ were used. Otherwise the maintenance of the preparation and the technique of recording and stimulation were as described previously ~-~ The effect of antidromic impulses in the L5-S1 ventral roots were tested on 34 disynaptic Ia IPSPs recorded in 22 different DSCT neurones. The IPSPs were * Present address: Department of Physiology, Dental School, Osaka University, 32 Joan-¢'ho. Kutaku, Osaka, Japan.
159 c o n s i d e r e d to o r i g i n a t e f r o m l a afferents if t h e y grew w i t h the first ([a) c o m p o n e n t o f the i n c o m i n g g r o u p I n e r v e volley ~ a n d to be d i s y n a p t i c if t h e y h a d
segmental
latencies less t h a n 1.0 m s e c ( m e a n 0.65 msec) l o n g e r t h a n the m o n o s y n a p t i c E P S P s in the cells 4. M o s t tested la 1PSPs w e r e e v o k e d f r o m the nerves to the knee e x t e n s o r q u a d r i c e p s (12) a n d the k n e e flexor p o s t e r i o r b i c e p s - s e m i t e n d i n o s u s (11), w h i c h h a v e b e e n m o s t extensively used in e a r l i e r studies
of recurrent
effects o n
la
IPSP
m o t o n e u r o n e s 6 and V S C T neuronesS, s. T h e l a I P S P s w e r e c o n d i t i o n e d by a single s t i m u l a t i o n o f the v e n t r a l roots, s u p r a m a x i m a l for a-fibres and p r e c e d i n g the test s t i m u l a t i o n by 8 - 1 0 msec. T h e r e was no case w i t h a r e c u r r e n t effect o n the l a 1PSP in the D S C T n e u r o n e s . A typical result is s h o w n in Fig. 1. A n 1PSP was e v o k e d in this cell f r o m the n e r v e to quadriceps.
The
IPSP appeared
w i t h the lowest t h r e s h o l d fibres (Fig.
IB) a n d
i n c r e a s e d in a m p l i t u d e w i t h t h e first (la) c o m p o n e n t o f the n e r v e volley (Fig. 1C), w i t h A |
DLF B
Q I.I
C
Q 1.5 D
Q 2.4
1
2.5 mVl
,---- I ms A - D
F
LS-SIVRs'~Q I.I G L5-SIVRs-~QI3
test.- ~
t
.
~
. ~
f
cond+ii~
| i1|
• t
1
f
1+5 ms PBSt
H
I
_ I ....
Q+PBSt
-
~.,!~,,,,~,,
d LS-L6VRs
.
.'~
:j K LS-L6VRs
•
.
I
1+5 ms H-K
f
I
Fig. 1. Lack of recurrent depression of la IPSPs in a DSCT neurone. Upper traces in A E are intracellular responses, lower traces are nerve volleys recorded triphasically from the dorsal root entry zone. Positivity is indicated upwards in intracellular recordings and downwards in nerve volley recordings. A : antidromic spikes evoked by stimulation of the dorsolateral funicle (DLF) of the ipsilateral side at the level of Th 12; B-D: disynaptic IPSPs evoked by la afferents in the quadriceps (Q) nerve; E : monosynaptic EPSP evoked by group I afferents in the sartorius nerve (Sart); F-G : averaged records of submaximal test la IPSPs evoked by stimulation of the Q nerve at two different strengths (upper traces) and test IPSPs conditioned by a preceding maximal a-volley in the L5 SI ventral roots (VRs; lower traces). Each trace is the average of 20 responses• The calibration pulses are 1 mV in amplitude and 2 msec in duration. The strength of the nerve stimulation in multiples of the threshold strength is indicated above the records in B-G. H K: monosynaptic reflexes recorded from the S1 ventral root (upper traces) and incoming nerve volleys as in B-E (lower traces). H: monosynaptic test reflex evoked by stimulation of the posterior biceps-semitendinosus nerve (PBSt); I: PBSt test reflex inhibited by a submaximal la volley in the quadriceps nerve (Q 1.15 × threshold); J : decreased la inhibition of the PBSt test reflex following a maximal a-volley in the L5-L6 ventral roots; K: direct effect of the L5-L6 ventral root volley on the PBSt test reflex. Arrows in F G and J K indicate the arrival of the ventral root volley to the spinal cord.
160 no further increase when the stimulus strength was increased to include also the seconu (ib) component of nerve volley (Fig. ID). The segmental latency of the IPSP was 1.4 msec as compared to 0,8 msec for the group 1 EPSP in the cell (Fig. 1E). Thus. this is ~ disynaptic la IPSP. The averaged records in Fig. I F and G show that the la IPSP was unaffected by a maximal a-volley in the L5--SI ventral roots. To ascertai~ that small recurrent effects were not overlooked, the conditioning procedure was repeated man\, times for each cell with test la IPSPs of different amplitudes. It was regularly controlled that ventral root volleys were effective m releasing motoneurones from la inhibition in these experiments. This was done with monosynaptic test reflexes as exemplified by the records in Fig. I H-K. taken .lust alter the records in Fig. I F-G. A monosynaptic test reflex was evoked by stimulamm of the posterior biceps-semitendinosus nerve (Fig. I H). This reflex was clearly decreased by a conditioning submaximal ia volley in the quadriceps nerve (Fig. 1I), but the inhibition was much less effective if the quadriceps nerve volley was preceded by a maximal a-volle~ in the L5-L6 ventral roots (Fig. 1J), The ventral root volley alone had no recurrent facilitatory effect on the posterior biceps-semitendinosus motoneurones tFig. t K}. This means that the increase in amplitude of the la inhibited reflex in J, as compared to the reflex in I, is the result of recurrent inhibition of the involved la inhibitorx interneurones~L Similar results were obtained in the other controls with le:-~t reflexe.~. Thus, the recurrent inhibitory pathway to la inhibitory mterneurones was operative in these experiments. Consequently the la inhibition of DSCT neuroneb must be mediated by other la inhibitory interneurones than those projecting to motoneurones and to some ventral spinocerebellar tract neurones. The present result has to be considered in relation to the possible function of the DSCT and the VSCT. It has recently been postulated that the VSCT signal information to cerebellum about the transmission in segmental reflex pathways to motoneurones 1°. This idea has received strong support by the demonstrmion of an inhibitory connexion to some VSCT neurones from the interneurones in the reciprocal Ia inhibitory pathway to motoneurones "~,a. Through this collateral connexion the VSCT will receive a measure of the activity in this particular reflex pathway 7, The DSCT, on the other hand, seems to be concerned primarily with peripheral events t'-', Most DSCT cells with excitation from muscle spindle la afferents receive inhibition from similar afferents in other muscle nerves, often in combinations which are not observed in motoneurones 9. This convergence indicates that the sensory inflow from several interacting muscles is integrated already at the level of the DSCT. A separate la inhibitory pathway to the DSCT would be appropriate if the inhibition represents an element in such a low level sensory integratiom This work was supported by the Swedish Medical Research Council (Project 04767) and by Wilhelm och Martina Lundgrens Vetenskapsfond.
1 Eccles, J, C., Eccles, R. M. and Lundberg, A., Synaptic actions on motoneurones in relation to the two components of the group I muscle afferent volley, J. Physiol. (Lond.), t36 (1957~ 527,--546.
161 2 Eccles, J. C., Fatt, P. and Landgren, S., The central pathway for the direct inhibitory action of impulses in the largest afferent nerve fibers to muscle, J. Neurophysiol., 19 (1956) 75 98. 3 Eccles, J. C., Hubbard, J. I. and Oscarsson, O., lntrace[lular recording from cells of the ventral spino-cerebellar tract, J. Physiol. (Lond.), 158 (1961) 486 516. 4 Eccles, J. C., Oscarsson, O. and Willis, W. D., Synaptic action of group l and I1 afferent fibres of muscle on the cells of the dorsal spino-cerebellar tract, J. Physiol. (Lond.), 158 (1961) 517 543. 5 Gustafsson, B. and Lindstr6m, S., Recurrent control from motor axon collaterals of Ia inhibitory pathways to ventral spinocerebellar tract neurones, Acta physiol, scamt., 89 (1973) 457 481. 6 Hultborn, H., Jankowska, E. and Lindstr6m, S., Recurrent inhibition from motor axon collaterals of transmission in the la inhibitory pathway to motoneurones, J. Physiol. (Lond.), 215 ([971) 591 612. 7 Lindstr6m, S., Recurrent control from motor axon collaterals of Ia inhibitory pathways in the spinal cord of the cat, Acta physiol, scand., Suppl. 392 (1973). 8 Lindstr6m, S. and Schomburg, E. D., Group I inhibition in Ib excited ventral spinocerebellar tract neurones, Acta physiol, scand., 90 (1974) 166 185. 9 Lindstr6m, S. and Takata, M., Convergence of excitation and inhibition in dorsal spinocerebellar tract neurones from group I afferents in hindlimb muscle nerves, To be published. 10 Lundberg, A., Function of the ventral spinocerebellar tract - - a new hypothesis, Exp. Braht Res., 12 (1971) 317 330. I 1 Lundberg, A. and Oscarsson, O., Functional organization of the dorsal spino-cerehellar tract in the cat. VII. Identification of units by antidromic activation from the cerebellar cortex with recognition of five functional subdivisions, Acta physiol, scand., 50 (1960) 356 374. 12 Oscarsson, O., Functional organization of spinocerebellar paths. In A. lggo (Ed.), Handbook of Sensoo' Physiology lI, Springer, Berlin, 1973, pp. 339-380.
Braht Re~earch, 129 (1977) 158 - I (~| ~: Elsevier/North-Holland Biomedical Press
Lack of recurrent depression from motor axon collaterals of la IPSPs in dorsal spinocerebellar tract neurones
SIVERT LINDSTROM and M1TSURU TAKATA*
Department of Physiology, University qf Giiteborg, GiJteborg (Sweden) (Accepted March 3rd, 1977)
Muscle spindle la afferents have disynaptic inhibitory connexions to several spinal neurones including motoneurones 2 and the cells of origin of the ventral (VSCT) 3 and dorsal (DSCT) 4 spinocerebellar tracts. In motoneurones ° and some VSCT cellsS, 8, the Ia IPSPs can be depressed by impulses in recurrent motor axon collaterals, indicating that the same la inhibitory interneurones project to both types of cells 5,7. Disynaptic Ia IPSPs in DSCT neurones have now been conditioned by a nerve volley in the ventral roots to determine whether the same group of ia interneurones terminate also on DSCT cells. The experiments were done on 6 cats anaesthetized with a-chloralose t50-60 mg/kg). Only preparations with a good threshold separation between la and lb afferents in the nerves from thigh muscles were used 1. lntracellular recordings were obtained from DSCT neurones in Clarke's column on the left side at the level of L3-L4. Most cells were identified as belonging to the DSCT by their location, and afferent input from muscle nerves and by antidromic activation from the ipsilateral dorsolateral funiculus at the level of Th 124. Some of the cells were identified by antidromic activation from the ipsilateral anterior lobe of cerebellum using unipolar cathodal surface stimulation with constant cm rent pulses with a duration of 0.2 msec and an intensity of less than 2 mA 11. In these latter experiments the dorsal funiculi and the right spinal half were transected at the level of Th t 2. Several muscle nerves to the left hindlimb (cf. ref. 5) and the left ventral roots L5-SI were transected and their proximal ends mounted for electrical stimulation. The incoming nerve volleys were recorded triphasically from the dorsal root entry zone in the caudal L6 segment. Microelectrodes filled with 2 M potassium cttrate and with tip diameter of 1.5-2.0 #m and resistance of 3-6 M ~ were used. Otherwise the maintenance of the preparation and the technique of recording and stimulation were as described previously ~-~ The effect of antidromic impulses in the L5-S1 ventral roots were tested on 34 disynaptic Ia IPSPs recorded in 22 different DSCT neurones. The IPSPs were * Present address: Department of Physiology, Dental School, Osaka University, 32 Joan-¢'ho. Kutaku, Osaka, Japan.
159 c o n s i d e r e d to o r i g i n a t e f r o m l a afferents if t h e y grew w i t h the first ([a) c o m p o n e n t o f the i n c o m i n g g r o u p I n e r v e volley ~ a n d to be d i s y n a p t i c if t h e y h a d
segmental
latencies less t h a n 1.0 m s e c ( m e a n 0.65 msec) l o n g e r t h a n the m o n o s y n a p t i c E P S P s in the cells 4. M o s t tested la 1PSPs w e r e e v o k e d f r o m the nerves to the knee e x t e n s o r q u a d r i c e p s (12) a n d the k n e e flexor p o s t e r i o r b i c e p s - s e m i t e n d i n o s u s (11), w h i c h h a v e b e e n m o s t extensively used in e a r l i e r studies
of recurrent
effects o n
la
IPSP
m o t o n e u r o n e s 6 and V S C T neuronesS, s. T h e l a I P S P s w e r e c o n d i t i o n e d by a single s t i m u l a t i o n o f the v e n t r a l roots, s u p r a m a x i m a l for a-fibres and p r e c e d i n g the test s t i m u l a t i o n by 8 - 1 0 msec. T h e r e was no case w i t h a r e c u r r e n t effect o n the l a 1PSP in the D S C T n e u r o n e s . A typical result is s h o w n in Fig. 1. A n 1PSP was e v o k e d in this cell f r o m the n e r v e to quadriceps.
The
IPSP appeared
w i t h the lowest t h r e s h o l d fibres (Fig.
IB) a n d
i n c r e a s e d in a m p l i t u d e w i t h t h e first (la) c o m p o n e n t o f the n e r v e volley (Fig. 1C), w i t h A |
DLF B
Q I.I
C
Q 1.5 D
Q 2.4
1
2.5 mVl
,---- I ms A - D
F
LS-SIVRs'~Q I.I G L5-SIVRs-~QI3
test.- ~
t
.
~
. ~
f
cond+ii~
| i1|
• t
1
f
1+5 ms PBSt
H
I
_ I ....
Q+PBSt
-
~.,!~,,,,~,,
d LS-L6VRs
.
.'~
:j K LS-L6VRs
•
.
I
1+5 ms H-K
f
I
Fig. 1. Lack of recurrent depression of la IPSPs in a DSCT neurone. Upper traces in A E are intracellular responses, lower traces are nerve volleys recorded triphasically from the dorsal root entry zone. Positivity is indicated upwards in intracellular recordings and downwards in nerve volley recordings. A : antidromic spikes evoked by stimulation of the dorsolateral funicle (DLF) of the ipsilateral side at the level of Th 12; B-D: disynaptic IPSPs evoked by la afferents in the quadriceps (Q) nerve; E : monosynaptic EPSP evoked by group I afferents in the sartorius nerve (Sart); F-G : averaged records of submaximal test la IPSPs evoked by stimulation of the Q nerve at two different strengths (upper traces) and test IPSPs conditioned by a preceding maximal a-volley in the L5 SI ventral roots (VRs; lower traces). Each trace is the average of 20 responses• The calibration pulses are 1 mV in amplitude and 2 msec in duration. The strength of the nerve stimulation in multiples of the threshold strength is indicated above the records in B-G. H K: monosynaptic reflexes recorded from the S1 ventral root (upper traces) and incoming nerve volleys as in B-E (lower traces). H: monosynaptic test reflex evoked by stimulation of the posterior biceps-semitendinosus nerve (PBSt); I: PBSt test reflex inhibited by a submaximal la volley in the quadriceps nerve (Q 1.15 × threshold); J : decreased la inhibition of the PBSt test reflex following a maximal a-volley in the L5-L6 ventral roots; K: direct effect of the L5-L6 ventral root volley on the PBSt test reflex. Arrows in F G and J K indicate the arrival of the ventral root volley to the spinal cord.
160 no further increase when the stimulus strength was increased to include also the seconu (ib) component of nerve volley (Fig. ID). The segmental latency of the IPSP was 1.4 msec as compared to 0,8 msec for the group 1 EPSP in the cell (Fig. 1E). Thus. this is ~ disynaptic la IPSP. The averaged records in Fig. I F and G show that the la IPSP was unaffected by a maximal a-volley in the L5--SI ventral roots. To ascertai~ that small recurrent effects were not overlooked, the conditioning procedure was repeated man\, times for each cell with test la IPSPs of different amplitudes. It was regularly controlled that ventral root volleys were effective m releasing motoneurones from la inhibition in these experiments. This was done with monosynaptic test reflexes as exemplified by the records in Fig. I H-K. taken .lust alter the records in Fig. I F-G. A monosynaptic test reflex was evoked by stimulamm of the posterior biceps-semitendinosus nerve (Fig. I H). This reflex was clearly decreased by a conditioning submaximal ia volley in the quadriceps nerve (Fig. 1I), but the inhibition was much less effective if the quadriceps nerve volley was preceded by a maximal a-volle~ in the L5-L6 ventral roots (Fig. 1J), The ventral root volley alone had no recurrent facilitatory effect on the posterior biceps-semitendinosus motoneurones tFig. t K}. This means that the increase in amplitude of the la inhibited reflex in J, as compared to the reflex in I, is the result of recurrent inhibition of the involved la inhibitorx interneurones~L Similar results were obtained in the other controls with le:-~t reflexe.~. Thus, the recurrent inhibitory pathway to la inhibitory mterneurones was operative in these experiments. Consequently the la inhibition of DSCT neuroneb must be mediated by other la inhibitory interneurones than those projecting to motoneurones and to some ventral spinocerebellar tract neurones. The present result has to be considered in relation to the possible function of the DSCT and the VSCT. It has recently been postulated that the VSCT signal information to cerebellum about the transmission in segmental reflex pathways to motoneurones 1°. This idea has received strong support by the demonstrmion of an inhibitory connexion to some VSCT neurones from the interneurones in the reciprocal Ia inhibitory pathway to motoneurones "~,a. Through this collateral connexion the VSCT will receive a measure of the activity in this particular reflex pathway 7, The DSCT, on the other hand, seems to be concerned primarily with peripheral events t'-', Most DSCT cells with excitation from muscle spindle la afferents receive inhibition from similar afferents in other muscle nerves, often in combinations which are not observed in motoneurones 9. This convergence indicates that the sensory inflow from several interacting muscles is integrated already at the level of the DSCT. A separate la inhibitory pathway to the DSCT would be appropriate if the inhibition represents an element in such a low level sensory integratiom This work was supported by the Swedish Medical Research Council (Project 04767) and by Wilhelm och Martina Lundgrens Vetenskapsfond.
1 Eccles, J, C., Eccles, R. M. and Lundberg, A., Synaptic actions on motoneurones in relation to the two components of the group I muscle afferent volley, J. Physiol. (Lond.), t36 (1957~ 527,--546.
161 2 Eccles, J. C., Fatt, P. and Landgren, S., The central pathway for the direct inhibitory action of impulses in the largest afferent nerve fibers to muscle, J. Neurophysiol., 19 (1956) 75 98. 3 Eccles, J. C., Hubbard, J. I. and Oscarsson, O., lntrace[lular recording from cells of the ventral spino-cerebellar tract, J. Physiol. (Lond.), 158 (1961) 486 516. 4 Eccles, J. C., Oscarsson, O. and Willis, W. D., Synaptic action of group l and I1 afferent fibres of muscle on the cells of the dorsal spino-cerebellar tract, J. Physiol. (Lond.), 158 (1961) 517 543. 5 Gustafsson, B. and Lindstr6m, S., Recurrent control from motor axon collaterals of Ia inhibitory pathways to ventral spinocerebellar tract neurones, Acta physiol, scamt., 89 (1973) 457 481. 6 Hultborn, H., Jankowska, E. and Lindstr6m, S., Recurrent inhibition from motor axon collaterals of transmission in the la inhibitory pathway to motoneurones, J. Physiol. (Lond.), 215 ([971) 591 612. 7 Lindstr6m, S., Recurrent control from motor axon collaterals of Ia inhibitory pathways in the spinal cord of the cat, Acta physiol, scand., Suppl. 392 (1973). 8 Lindstr6m, S. and Schomburg, E. D., Group I inhibition in Ib excited ventral spinocerebellar tract neurones, Acta physiol, scand., 90 (1974) 166 185. 9 Lindstr6m, S. and Takata, M., Convergence of excitation and inhibition in dorsal spinocerebellar tract neurones from group I afferents in hindlimb muscle nerves, To be published. 10 Lundberg, A., Function of the ventral spinocerebellar tract - - a new hypothesis, Exp. Braht Res., 12 (1971) 317 330. I 1 Lundberg, A. and Oscarsson, O., Functional organization of the dorsal spino-cerehellar tract in the cat. VII. Identification of units by antidromic activation from the cerebellar cortex with recognition of five functional subdivisions, Acta physiol, scand., 50 (1960) 356 374. 12 Oscarsson, O., Functional organization of spinocerebellar paths. In A. lggo (Ed.), Handbook of Sensoo' Physiology lI, Springer, Berlin, 1973, pp. 339-380.