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Recurrent inhibition from motor axon collaterals in interneurones monosynaptically activated from la afferents
367
SHORT COMMUNICATIONS
Recurrent inhibition from motor axon collaterals in interneurones monosynaptically activated from, la afferents An investigation of recurrent effects from motor axon collaterals on reflex transmission to motoneurones revealed a selective inhibition in the reciprocal disynaptic la inhibitory pathway. By all criteria this inhibition appeared to be caused by recurrent inhibition of la inhibitory interneurones4,L In the present study we have explored the spinal cord in search of interneurones with convergence of inhibition from motor axon collaterals and monosynaptic la excitation. Two regions were explored systematically: (a) the intermediate nucleus in which many interneurones are monosynaptically excited from la afferents 1 and have been assumed to mediate the la inhibition from antagonists z and (b) the ventral horn where interneurones with recurrent inhibition (otherwise unidentified) have been foundS, 9 and where some interneurones excited from group la afferents are also located.
A
C
A B S m 1.04
B
0.1 + 0.5
~ ....
msec
ABSm
r.=-"--
~ ....
D
J ....
J
....
VR L 7 J-AEISm
q mm w, T 1+5
E
1.9
msec
spont
J
F
VR L7 +spont
I mV •. . r--
10+50
msec I ,
.
,
.
,
IIII
.
,
I
,
,
__
I
I
I
Fig. 1. Extracellular recording from an interneurone (upper traces) in L6 at a depth of 3.38 mm from the cord dorsum (of. filled circle in Fig. 2F). Lower traces are from L6 dorsal root entry zone. In the upper traces negativity is signalled downwards and in the lower traces upwards. A-C, monosynaptic spike potentials evoked by stimulating the nerve to anterior biceps and semimembranosus (ABSm), strengths indicated above the records in multiples of threshold. The interneurone was excited by stimulating the lowest threshold group I afferent fibres (cf. incoming volleys in A, at threshold for the nerve, and in B, at group I maximal strength). D, inhibition of the group I excitation by preceding stimulation of the L7 ventral root (VR). The test alone is shown in C. E, resting activity of the cell and F, its inhibition by stimulation of the L7 ventral root. All the records consist of 10 superimposed traces. The voltage calibration in D is for A - D and in F for E-F. Spinal cat, anaemically decorticated and under light Nembutal anaesthesia (10 mg/kg).
Brain Research, 9 (1968) 367-369
368
SHORT COMMUNICATIONS In the intermediate nucleus we failed to detect a n y recurrent i n h i b i t o r y actions
o n i n t e r n e u r o n e s excited either by the lowest threshold g r o u p I muscle afferents or by other afferents. However, in the ventral horn we f o u n d 29 i n t e r n e u r o n e s with a convergence of m o n o s y n a p t i c excitation from group Ia afferents and i n h i b i t i o n by antidromic s t i m u l a t i o n of ventral roots. These cells were f o u n d outside but close to the m o t o r nucleus. The possibility that the records were obtained from m o t o n e u r o n a l dendrites was considered b u t careful testing with both extra- and intracellutar recording revealed that the cells could n o t be antidromically i n v a d e d ; furthermore, reciprocal Ia IPSPs characteristic for m o t o n e u r o n e s were never found in them. Figs. 1 a n d 2 show one of these i n t e r n e u r o n e s recorded both extra- a n d intracellullarty. Extracellular records such as in Fig. 1 show recurrent i n h i b i t i o n of both the resting activity a n d of the responses evoked by s t i m u l a t i n g low threshold group I afferents. T h e intracellular records revealed m o n o s y n a p t i c EPSPs from g r o u p la afferents a n d recurrent IPSPs with a latency of 1.6-1.8 msec and a d u r a t i o n of a b o u t 50 msec. Most of these i n t e r n e u r o n e s received m o n o s y n a p t i c excitation from one muscle nerve only.
~
D
A B S mA1.08 B
, ~ R
L7
E
.,. 13 ~
~
VR L7
I r~ec
1*5 msec Fig. 2, Intracellular records (upper traces) from the same interneurone as illustrated in Fig. L The lower traces in A-D and the middle trace in E are from L6 dorsal root entry zone. The lowermost trace in E is the field potential recorded after withdrawal of the electrode to a just extracellular position. A-C. monosynaptic EPSPs evoked by stimulating the nerve to ABSm with strengths slightly above threshold (A), submaximal for group I afferents (B) and maximal for group I (C). As the EPSP is evoked from the lowest threshold group I afferents and its amplitude is not increased from B to C when higher threshold group I afferents are added, it is postulated that the EPSP is evoked from Ia afferents alone. D and E, IPSPs evoked by stimulating the L7 VR with the strength in D being submaximal for alpha afferents. D shows the latency of the IPSP while E, at slow sweep speed and long amplifier time constant (0.8 sec), indicates its duration. Time and voltage calibrations in D are for A-D and in E for E (note different amplification of the intracellular and extracellular record). F, location of 10 interneurones with convergence of Ia monosynaptic excitation and recurrent inhibition. The interneuroneillustrated is marked by a filled circle. All these interneuroneswere found in one experiment in the L6 segment. The explored area was 200 # medially and laterally and about 1.0 mm rostrally and caudally from the electrode track drawn from serial histological sections. Points. motoneurone somas stained (Nissl) in the sections with the electrode track. Hatched areas, the motor and intermediate nuclei, the latter with group I potentials from quadriceps, anterior biceps and semimembranosus and sartorius. Brain Research, 9 (1968) 367-369
SHORT COMMUNICATIONS
369
In 5 cells o f 6 in which descending effects were investigated with intracellular recording, m o n o s y n a p t i c EPSPs were evoked by s t i m u l a t i o n o f the dissected ventral q u a d r a n t o f the spinal cord in the lower thoracic region. This is o f interest as it has been shown by G r i l l n e r et al. a that impulses in p a t h w a y s descending in the ventral q u a d r a n t (vestibulo- a n d reticulospinal) facilitate la inhibition t h r o u g h m o n o s y n a p t i c excitatory action at an i n t e r n e u r o n a l level. It should also be noted t h a t they did not find any descending excitatory action from these p a t h w a y s in la interneurones located in the i n t e r m e d i a t e nucleus. All the interneurones in the present study were found d o r s o m e d i a l to the m o t o r nuclei (Fig. 2F), in the ventral part o f Rexed's l a m i n a VI ! 6. The l o c a t i o n c o r r e s p o n d s well with the ventral a r e a o f terminal b r a n c h i n g o f Ia afferents outside the m o t o n e u r o n e pool described by SzentS.gothai 7. To s u m m a r i z e : The interneurones here described are characterized by a convergence o f m o n o s y n a p t i c la excitation, recurrent IPSPs from m o t o r axon collaterals and, in some cases, m o n o s y n a p t i c excitation from descending ventral spinal pathways. This pattern o f convergence strongly suggests that they mediate the reciprocal l a inh i b i t i o n to m o t o n e u r o n e s . Department of Physiology, University of GOteborg, G6teborg f Sweden)
H. H U LTBO RN E. JANKOWSKA S. L1N DSTROM
1 EccLws, J. C., ECCLES,R. M., AYD LtrNDBER~,A., Types of neurone in and around the intermediate nucleus of the lumbosacral cord, J. Physiol. (Lond.), 154 (1969) 89-114. 2 ECCLES,J. C., FAvr, P., Ay• LANDGREN, S., The central pathway for the direct inhibitory action of impulses in the largest afferent nerve fibres to muscles, J. Neurop#ysiol., 19 (1956) 75 98. 3 GRILLNER,S., HONGO, T., AND LUND, S., Interaction between the inhibitory pathways from the Deiters' nucleus and Ia afferents to flexor motoneurones, Acta physiol, scand., 68, Suppl. 277 (1966) 61. 4 HULTBORN, H., JANKOWSKA, E., AND LINDSTROM, S., Inhibition in la inhibitory pathway by impulses in recurrent motor axon collaterals, Life Sci., 7 (1968) 337 339. 5 HULTBORN,H., JANKOWSKA,E., AND L~NDSTR~3M,S., Recurrent inhibition of reflex transmission to motoneurones, Acta physiol, scand., (1968). In press. 6 REXED, B., A cytoarchitectonic atlas of the spinal cord in the cat, J. comp. Neurol., 100 (1954) 297-379. 7 SZENT,~GOTHAI,J., Synaptic architecture of the spinal motoneuron pool, Electroenceph. olin. Neurophysiol., Suppl. 25 (1967) 4-23. 8 WILLIS,W. D., AND WILLlS,J. C., Properties of interneurons in the ventral spinal cord, Arch. ital. Biol., 104 (1966) 354-386. 9 WILSON,V. J., AND BURGESS, P., Effects of antidromic conditioning on some motoneurons and interneurons, J. Neurophysiol., 25 (1962) 636-650. (Accepted April l lth, 1968)
Brain Research, 9 (1968) 367-369
SHORT COMMUNICATIONS
Recurrent inhibition from motor axon collaterals in interneurones monosynaptically activated from, la afferents An investigation of recurrent effects from motor axon collaterals on reflex transmission to motoneurones revealed a selective inhibition in the reciprocal disynaptic la inhibitory pathway. By all criteria this inhibition appeared to be caused by recurrent inhibition of la inhibitory interneurones4,L In the present study we have explored the spinal cord in search of interneurones with convergence of inhibition from motor axon collaterals and monosynaptic la excitation. Two regions were explored systematically: (a) the intermediate nucleus in which many interneurones are monosynaptically excited from la afferents 1 and have been assumed to mediate the la inhibition from antagonists z and (b) the ventral horn where interneurones with recurrent inhibition (otherwise unidentified) have been foundS, 9 and where some interneurones excited from group la afferents are also located.
A
C
A B S m 1.04
B
0.1 + 0.5
~ ....
msec
ABSm
r.=-"--
~ ....
D
J ....
J
....
VR L 7 J-AEISm
q mm w, T 1+5
E
1.9
msec
spont
J
F
VR L7 +spont
I mV •. . r--
10+50
msec I ,
.
,
.
,
IIII
.
,
I
,
,
__
I
I
I
Fig. 1. Extracellular recording from an interneurone (upper traces) in L6 at a depth of 3.38 mm from the cord dorsum (of. filled circle in Fig. 2F). Lower traces are from L6 dorsal root entry zone. In the upper traces negativity is signalled downwards and in the lower traces upwards. A-C, monosynaptic spike potentials evoked by stimulating the nerve to anterior biceps and semimembranosus (ABSm), strengths indicated above the records in multiples of threshold. The interneurone was excited by stimulating the lowest threshold group I afferent fibres (cf. incoming volleys in A, at threshold for the nerve, and in B, at group I maximal strength). D, inhibition of the group I excitation by preceding stimulation of the L7 ventral root (VR). The test alone is shown in C. E, resting activity of the cell and F, its inhibition by stimulation of the L7 ventral root. All the records consist of 10 superimposed traces. The voltage calibration in D is for A - D and in F for E-F. Spinal cat, anaemically decorticated and under light Nembutal anaesthesia (10 mg/kg).
Brain Research, 9 (1968) 367-369
368
SHORT COMMUNICATIONS In the intermediate nucleus we failed to detect a n y recurrent i n h i b i t o r y actions
o n i n t e r n e u r o n e s excited either by the lowest threshold g r o u p I muscle afferents or by other afferents. However, in the ventral horn we f o u n d 29 i n t e r n e u r o n e s with a convergence of m o n o s y n a p t i c excitation from group Ia afferents and i n h i b i t i o n by antidromic s t i m u l a t i o n of ventral roots. These cells were f o u n d outside but close to the m o t o r nucleus. The possibility that the records were obtained from m o t o n e u r o n a l dendrites was considered b u t careful testing with both extra- and intracellutar recording revealed that the cells could n o t be antidromically i n v a d e d ; furthermore, reciprocal Ia IPSPs characteristic for m o t o n e u r o n e s were never found in them. Figs. 1 a n d 2 show one of these i n t e r n e u r o n e s recorded both extra- a n d intracellullarty. Extracellular records such as in Fig. 1 show recurrent i n h i b i t i o n of both the resting activity a n d of the responses evoked by s t i m u l a t i n g low threshold group I afferents. T h e intracellular records revealed m o n o s y n a p t i c EPSPs from g r o u p la afferents a n d recurrent IPSPs with a latency of 1.6-1.8 msec and a d u r a t i o n of a b o u t 50 msec. Most of these i n t e r n e u r o n e s received m o n o s y n a p t i c excitation from one muscle nerve only.
~
D
A B S mA1.08 B
, ~ R
L7
E
.,. 13 ~
~
VR L7
I r~ec
1*5 msec Fig. 2, Intracellular records (upper traces) from the same interneurone as illustrated in Fig. L The lower traces in A-D and the middle trace in E are from L6 dorsal root entry zone. The lowermost trace in E is the field potential recorded after withdrawal of the electrode to a just extracellular position. A-C. monosynaptic EPSPs evoked by stimulating the nerve to ABSm with strengths slightly above threshold (A), submaximal for group I afferents (B) and maximal for group I (C). As the EPSP is evoked from the lowest threshold group I afferents and its amplitude is not increased from B to C when higher threshold group I afferents are added, it is postulated that the EPSP is evoked from Ia afferents alone. D and E, IPSPs evoked by stimulating the L7 VR with the strength in D being submaximal for alpha afferents. D shows the latency of the IPSP while E, at slow sweep speed and long amplifier time constant (0.8 sec), indicates its duration. Time and voltage calibrations in D are for A-D and in E for E (note different amplification of the intracellular and extracellular record). F, location of 10 interneurones with convergence of Ia monosynaptic excitation and recurrent inhibition. The interneuroneillustrated is marked by a filled circle. All these interneuroneswere found in one experiment in the L6 segment. The explored area was 200 # medially and laterally and about 1.0 mm rostrally and caudally from the electrode track drawn from serial histological sections. Points. motoneurone somas stained (Nissl) in the sections with the electrode track. Hatched areas, the motor and intermediate nuclei, the latter with group I potentials from quadriceps, anterior biceps and semimembranosus and sartorius. Brain Research, 9 (1968) 367-369
SHORT COMMUNICATIONS
369
In 5 cells o f 6 in which descending effects were investigated with intracellular recording, m o n o s y n a p t i c EPSPs were evoked by s t i m u l a t i o n o f the dissected ventral q u a d r a n t o f the spinal cord in the lower thoracic region. This is o f interest as it has been shown by G r i l l n e r et al. a that impulses in p a t h w a y s descending in the ventral q u a d r a n t (vestibulo- a n d reticulospinal) facilitate la inhibition t h r o u g h m o n o s y n a p t i c excitatory action at an i n t e r n e u r o n a l level. It should also be noted t h a t they did not find any descending excitatory action from these p a t h w a y s in la interneurones located in the i n t e r m e d i a t e nucleus. All the interneurones in the present study were found d o r s o m e d i a l to the m o t o r nuclei (Fig. 2F), in the ventral part o f Rexed's l a m i n a VI ! 6. The l o c a t i o n c o r r e s p o n d s well with the ventral a r e a o f terminal b r a n c h i n g o f Ia afferents outside the m o t o n e u r o n e pool described by SzentS.gothai 7. To s u m m a r i z e : The interneurones here described are characterized by a convergence o f m o n o s y n a p t i c la excitation, recurrent IPSPs from m o t o r axon collaterals and, in some cases, m o n o s y n a p t i c excitation from descending ventral spinal pathways. This pattern o f convergence strongly suggests that they mediate the reciprocal l a inh i b i t i o n to m o t o n e u r o n e s . Department of Physiology, University of GOteborg, G6teborg f Sweden)
H. H U LTBO RN E. JANKOWSKA S. L1N DSTROM
1 EccLws, J. C., ECCLES,R. M., AYD LtrNDBER~,A., Types of neurone in and around the intermediate nucleus of the lumbosacral cord, J. Physiol. (Lond.), 154 (1969) 89-114. 2 ECCLES,J. C., FAvr, P., Ay• LANDGREN, S., The central pathway for the direct inhibitory action of impulses in the largest afferent nerve fibres to muscles, J. Neurop#ysiol., 19 (1956) 75 98. 3 GRILLNER,S., HONGO, T., AND LUND, S., Interaction between the inhibitory pathways from the Deiters' nucleus and Ia afferents to flexor motoneurones, Acta physiol, scand., 68, Suppl. 277 (1966) 61. 4 HULTBORN, H., JANKOWSKA, E., AND LINDSTROM, S., Inhibition in la inhibitory pathway by impulses in recurrent motor axon collaterals, Life Sci., 7 (1968) 337 339. 5 HULTBORN,H., JANKOWSKA,E., AND L~NDSTR~3M,S., Recurrent inhibition of reflex transmission to motoneurones, Acta physiol, scand., (1968). In press. 6 REXED, B., A cytoarchitectonic atlas of the spinal cord in the cat, J. comp. Neurol., 100 (1954) 297-379. 7 SZENT,~GOTHAI,J., Synaptic architecture of the spinal motoneuron pool, Electroenceph. olin. Neurophysiol., Suppl. 25 (1967) 4-23. 8 WILLIS,W. D., AND WILLlS,J. C., Properties of interneurons in the ventral spinal cord, Arch. ital. Biol., 104 (1966) 354-386. 9 WILSON,V. J., AND BURGESS, P., Effects of antidromic conditioning on some motoneurons and interneurons, J. Neurophysiol., 25 (1962) 636-650. (Accepted April l lth, 1968)
Brain Research, 9 (1968) 367-369