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Analysis of a trigemino-abducens reflex in the cat
SHORT COMMUNICATIONS
313
Analysis of a trigemino-abducens reflex in the cat Aim of this investigation was to study the reflex organization in the VIth nerve. In nembutalized and curarized cats the abducens nerve of one side was exposed at its exit from the brain-stem after removal of the larynx and tongue and opening of the occipital bone lamina: then the mandibular bone of the same side was removed together with the palatine bone and the orbital cavity opened in order to dissect the eye muscles and their nerves. With the aid of a dissection microscope the following nerves of the same side were prepared and mounted on bipolar silver electrodes: the abducens (VIth) nerve, cut at the greatest possible distance from its exit from the medulla, the rectus lateralis nerve (RL), the infraorbital (IO) and the supraorbital (SO) nerves In some experiments the Vlth nerve was split in two branches: one was stimulated while recording took place from the other. In some other, single fiber activity was recorded from the VIth nerve after dissection of its rootlets. In another group of animals receiving Nembutal but not curare, extrinsic eye muscles were dissected free and their electrical activity evoked by IO stimulation recorded with Ag-AgC1 electrodes. A 10
IO -~.--
Vlth ~'~.-2.2
1.2 ~
,~
,--~\'~.
V--f'X~-.
,
15(
B 13(
17 tO 9O
70.
Fig. 1. A, The abducens nerve response (VIth) to infraorbital nerve stimulation and the afferent volley (IO) recorded from a filament of the IO nerve are shown. Numbers on the left indicate stimulus intensity expressed as multiples of the threshold. B, Represents the interaction phenomena between IO and SO volleys. In the abscissa: intervals between IO and SO stimulation, the latter being delivered at the origin of abscissa. In the ordinate: percentage variations of the size of the reflex response evoked by IO stimulation. C, In the upper traces the IO evoked responses in the abducens nerve are shown with different time basis (test); in the lower traces the same responses were preceded by an SO volley at 2.7 (left) and 26 (right) msec interval (cond). Time calibration: I msec. Amplitude calibration:
200#v. Brain Research, 7 (1968) 313-316
314
SHORT COMMUNICATIONS
Under our experimental conditions we could never record any reflex response to R L stimulation in the central stump of the dissected Vlth nerve. IO single shock stimulation evoked in the abducens nerve a polyphasic reflex response with a latency of 2.8-5 msec. As the stimulus strength was raised, this response increased in amplitude while its latency shortened (Fig. I A). Recording the afferent volley from a dissected filament o f IO nerve has indicated that the threshold for evoking this reflex was identical to that o f group A IO fibers 4 (Fig. 1A). Reflex activity evoked by IO stimulation was also recorded from single abducens fibers. Units have been registered which were activated by trigeminal volleys with a variable latency (3-8 msec). They could respond either with one impulse or with bursts of 2-4 impulses (Fig. 2). Under our experimental conditions units activated by IO stimulation did not generally show any spontaneous activity. Some which discharged spontaneously were not fired by trigeminal volleys. SO single shock stimulation generally gave no detectable responses in the Vlth nerve. Sometimes, however, a small potential could be evoked by SO repetitive (3-4 imp. at 300/sec) stimulation. When SO stimuli either preceded or followed IO activation, interaction p h e n o m e n a could be observed. Fig. IB shows that the IO evoked reflex increases in amplitude when the test stimulus precedes the conditioning SO shock by 4-0 msec or follows it by from 0 to about 10 msec. Maximal effect was obtained at 3-4 msec S O - 1 0 interval. When this interval was increased to over 10 msec, the IO reflex amplitude decreased for about 100-120 msec with a maximum effect at 20-25 msec. The same effects were seen while recording from a single abducens filament (Fig. 2). In the experiments in which the abducens nerve was dissected in two parts single or repetitive stimulation of one branch could never induce a reflex response on the other. This stimulation also never affected the amplitude o f the reflex response induced in the other branch by IO stimulation.
latency
B
msec
,,,~t~L
8 i
o°
°°
Ol
mn
mm
II
0
0
0
0
0
0
0
o
4 2 .
4
?
.
2
.
.
.
4
.
.
.
6
.
.
8
.
, _
10
12
J
msec
Fig. 2. A, Activity in a single abducens fiber evoked by single shock stimulation of IO nerve. In B, the same response is shown when the SO nerve is stimulated 4 msec before the IO nerve. Note facilitation of reflex unitary response as indicated by reduction of latency and increase in number of spikes. In the graph the time course of the latency variations of unitary response in the Vlth nerve to IO volley is indicated. Abscissa: SO-IO intervals; O indicates SO stimulation. Ordinate gives latency in msec. After 13 msec no unitary response could be evoked. Brain Research, 7 (1968) 313-316
SHORT COMMUNICATIONS
315
In a group of animals given Nembutal without curare the IO reflex responses were recorded from the muscles supplied by the Vlth nerve, i.e. the lateral head of the retractor oculi (RO) (see McCough and Adler 6 for references) and the rectus lateralis muscle (RL). In such conditions liminar stimulation of the IO nerve evoked in RO muscle a reflex response with I0--11 msec latency. By augmenting the stimulus strength an increase of the reflex amplitude was observed, while the latency decreased to 5-6 msec. No potential changes were observed in the RL muscle until stimulus intensity was 5 times the threshold to evoke RO reflex. At this or higher stimulus intensity only very small potentials could be recorded from the R L muscle (Fig. 3). RO 1.0
.~--J~-~
RL I
'- "
'-
_ _ . .
5.0 •
•
°
•
•
•
.
•
o
•
Fig. 3. Myographic responses of the retractor oculi (RO) and of the rectus lateralis (RL) muscles induced by IO nerve stimulation at the intensities indicated as multiples of the threshold by the numbers on the left. Time calibration: 5 msec. Voltage calibration: 200/~V. Our results indicate that in nembutalized cats RL nerve stimuli cannot evoke any reflex response in the central stump of the abducens nerve. This would suggest that the proprioceptive afferences from rectus lateralis muscle run in the abducens nerve itself as suggested by Tozer and Sherrington s, Bach-y-Rita and Murata 1 and Palmieri and Asole 7. However, stimulation of one branch of the Vlth nerve did not evoke any reflex response in the other one. This could be explained by admitting that under Nembutal anesthesia stimulation of afferent fibers from ocular muscles, which possibly run in the abducens nerve, is not able to give supraliminar excitation of Vlth nerve motoneurons. However, the hypothesis that these afferences enter the central nervous system by other way than the abducens nerve cannot be ruled out. The electromyographic observation that IO stimulation evoked a reflex response exclusively in RO muscle indicates that the reflex recorded from the Vlth nerve was entirely due to excitation of motoneurons which supply RO muscles. This RO reflex is therefore the electrophysiological equivalent of the retraction reflex 6 inducible by touching the conjunctive in decerebrated cat. The S O - I O interaction phenomena can be interpreted as a facilitatory convergence of two excitatory volleys upon a c o m m o n neuronal pool, followed by an Brain Research, 7 (1968) 313-316
316
SHORT COMMUNICATIONS
i n h i b i t i o n w h o s e t i m e c o u r s e was s i m i l a r to t h a t o f p r e s y n a p t i c i n h i b i t i o n b e t w e e n t r i g e m i n a l afferents d e s c r i b e d by D a r i a n - S m i t h 3. F i n a l l y , t h e a b s e n c e in o u r experim e n t s o f a n y r e c u r r e n t effect o n the V l t h n e r v e seems to c o n f i r m t h e a n a t o m i c a l o b s e r v a t i o n o f C a j a l z a n d L o r e n t e de N 6 ~ t h a t o c u l a r m o t o n e u r o n s are n o t p r o v i d e d w i t h r e c u r r e n t collaterals. Istituto di Fisiologia Umana dell'Universit& di Milano and lmpresa di Elettrofisiologia del CNR, Sezione di Milano, Milan (Italy)
FAUSTO BALDISSERA GIOVANNI BROGGI
I BACH-Y-RITA, P., AND MURATA, K., Extra-ocular proprioceptive receptors in VI nerve of cat, Quart. J. exp. Physiol., 49 (1964) 408-416. 2 CAJAL,S. RAM6N Y, Histologie du Systdme Nerveux de I'Homme et des Vertdbrds, Maloine, Paris, 1909, Vol. 1, XV, 986 pp. 3 DARIAN-SMITH, I., Presynaptic component in the afferent inhibition observed within trigeminal brain stem nuclei of the cat, J. Neurophysiol., 28 (1965) 695-709. 4 GASSER, H. S., AND ERLANGER, J., Electrical Signs o f Nervous Actions, Pennsylvania University Press, Philadelphia, 1937. 5 LORENTEDE NO, R., Action potentials of the motoneurons of the hypoglossus nucleus, J. cell. comp. Physiol., 29 (1947) 207-287. 6 McCoucH, G. P., AND ADLER, F. M., Extraocular reflexes, Amer. J. Physiol., 100 (1932) 78-88. 7 PALMIERI,G., AND ASOLE, A., On the presence of ganglion cells in the eye muscle nerves of some mammals and birds, Riv. Biol., 60 (1967) 139-152. 8 TOZER, F. M., AND SHERR~NGTON,C. S., Receptors and afferents of the third, fourth and sixth cranial nerves, Proc. roy. Soc. B., 82 (1910)450-457. (Accepted October 24th, 1967)
Brain Research, 7 (1968) 313-316
313
Analysis of a trigemino-abducens reflex in the cat Aim of this investigation was to study the reflex organization in the VIth nerve. In nembutalized and curarized cats the abducens nerve of one side was exposed at its exit from the brain-stem after removal of the larynx and tongue and opening of the occipital bone lamina: then the mandibular bone of the same side was removed together with the palatine bone and the orbital cavity opened in order to dissect the eye muscles and their nerves. With the aid of a dissection microscope the following nerves of the same side were prepared and mounted on bipolar silver electrodes: the abducens (VIth) nerve, cut at the greatest possible distance from its exit from the medulla, the rectus lateralis nerve (RL), the infraorbital (IO) and the supraorbital (SO) nerves In some experiments the Vlth nerve was split in two branches: one was stimulated while recording took place from the other. In some other, single fiber activity was recorded from the VIth nerve after dissection of its rootlets. In another group of animals receiving Nembutal but not curare, extrinsic eye muscles were dissected free and their electrical activity evoked by IO stimulation recorded with Ag-AgC1 electrodes. A 10
IO -~.--
Vlth ~'~.-2.2
1.2 ~
,~
,--~\'~.
V--f'X~-.
,
15(
B 13(
17 tO 9O
70.
Fig. 1. A, The abducens nerve response (VIth) to infraorbital nerve stimulation and the afferent volley (IO) recorded from a filament of the IO nerve are shown. Numbers on the left indicate stimulus intensity expressed as multiples of the threshold. B, Represents the interaction phenomena between IO and SO volleys. In the abscissa: intervals between IO and SO stimulation, the latter being delivered at the origin of abscissa. In the ordinate: percentage variations of the size of the reflex response evoked by IO stimulation. C, In the upper traces the IO evoked responses in the abducens nerve are shown with different time basis (test); in the lower traces the same responses were preceded by an SO volley at 2.7 (left) and 26 (right) msec interval (cond). Time calibration: I msec. Amplitude calibration:
200#v. Brain Research, 7 (1968) 313-316
314
SHORT COMMUNICATIONS
Under our experimental conditions we could never record any reflex response to R L stimulation in the central stump of the dissected Vlth nerve. IO single shock stimulation evoked in the abducens nerve a polyphasic reflex response with a latency of 2.8-5 msec. As the stimulus strength was raised, this response increased in amplitude while its latency shortened (Fig. I A). Recording the afferent volley from a dissected filament o f IO nerve has indicated that the threshold for evoking this reflex was identical to that o f group A IO fibers 4 (Fig. 1A). Reflex activity evoked by IO stimulation was also recorded from single abducens fibers. Units have been registered which were activated by trigeminal volleys with a variable latency (3-8 msec). They could respond either with one impulse or with bursts of 2-4 impulses (Fig. 2). Under our experimental conditions units activated by IO stimulation did not generally show any spontaneous activity. Some which discharged spontaneously were not fired by trigeminal volleys. SO single shock stimulation generally gave no detectable responses in the Vlth nerve. Sometimes, however, a small potential could be evoked by SO repetitive (3-4 imp. at 300/sec) stimulation. When SO stimuli either preceded or followed IO activation, interaction p h e n o m e n a could be observed. Fig. IB shows that the IO evoked reflex increases in amplitude when the test stimulus precedes the conditioning SO shock by 4-0 msec or follows it by from 0 to about 10 msec. Maximal effect was obtained at 3-4 msec S O - 1 0 interval. When this interval was increased to over 10 msec, the IO reflex amplitude decreased for about 100-120 msec with a maximum effect at 20-25 msec. The same effects were seen while recording from a single abducens filament (Fig. 2). In the experiments in which the abducens nerve was dissected in two parts single or repetitive stimulation of one branch could never induce a reflex response on the other. This stimulation also never affected the amplitude o f the reflex response induced in the other branch by IO stimulation.
latency
B
msec
,,,~t~L
8 i
o°
°°
Ol
mn
mm
II
0
0
0
0
0
0
0
o
4 2 .
4
?
.
2
.
.
.
4
.
.
.
6
.
.
8
.
, _
10
12
J
msec
Fig. 2. A, Activity in a single abducens fiber evoked by single shock stimulation of IO nerve. In B, the same response is shown when the SO nerve is stimulated 4 msec before the IO nerve. Note facilitation of reflex unitary response as indicated by reduction of latency and increase in number of spikes. In the graph the time course of the latency variations of unitary response in the Vlth nerve to IO volley is indicated. Abscissa: SO-IO intervals; O indicates SO stimulation. Ordinate gives latency in msec. After 13 msec no unitary response could be evoked. Brain Research, 7 (1968) 313-316
SHORT COMMUNICATIONS
315
In a group of animals given Nembutal without curare the IO reflex responses were recorded from the muscles supplied by the Vlth nerve, i.e. the lateral head of the retractor oculi (RO) (see McCough and Adler 6 for references) and the rectus lateralis muscle (RL). In such conditions liminar stimulation of the IO nerve evoked in RO muscle a reflex response with I0--11 msec latency. By augmenting the stimulus strength an increase of the reflex amplitude was observed, while the latency decreased to 5-6 msec. No potential changes were observed in the RL muscle until stimulus intensity was 5 times the threshold to evoke RO reflex. At this or higher stimulus intensity only very small potentials could be recorded from the R L muscle (Fig. 3). RO 1.0
.~--J~-~
RL I
'- "
'-
_ _ . .
5.0 •
•
°
•
•
•
.
•
o
•
Fig. 3. Myographic responses of the retractor oculi (RO) and of the rectus lateralis (RL) muscles induced by IO nerve stimulation at the intensities indicated as multiples of the threshold by the numbers on the left. Time calibration: 5 msec. Voltage calibration: 200/~V. Our results indicate that in nembutalized cats RL nerve stimuli cannot evoke any reflex response in the central stump of the abducens nerve. This would suggest that the proprioceptive afferences from rectus lateralis muscle run in the abducens nerve itself as suggested by Tozer and Sherrington s, Bach-y-Rita and Murata 1 and Palmieri and Asole 7. However, stimulation of one branch of the Vlth nerve did not evoke any reflex response in the other one. This could be explained by admitting that under Nembutal anesthesia stimulation of afferent fibers from ocular muscles, which possibly run in the abducens nerve, is not able to give supraliminar excitation of Vlth nerve motoneurons. However, the hypothesis that these afferences enter the central nervous system by other way than the abducens nerve cannot be ruled out. The electromyographic observation that IO stimulation evoked a reflex response exclusively in RO muscle indicates that the reflex recorded from the Vlth nerve was entirely due to excitation of motoneurons which supply RO muscles. This RO reflex is therefore the electrophysiological equivalent of the retraction reflex 6 inducible by touching the conjunctive in decerebrated cat. The S O - I O interaction phenomena can be interpreted as a facilitatory convergence of two excitatory volleys upon a c o m m o n neuronal pool, followed by an Brain Research, 7 (1968) 313-316
316
SHORT COMMUNICATIONS
i n h i b i t i o n w h o s e t i m e c o u r s e was s i m i l a r to t h a t o f p r e s y n a p t i c i n h i b i t i o n b e t w e e n t r i g e m i n a l afferents d e s c r i b e d by D a r i a n - S m i t h 3. F i n a l l y , t h e a b s e n c e in o u r experim e n t s o f a n y r e c u r r e n t effect o n the V l t h n e r v e seems to c o n f i r m t h e a n a t o m i c a l o b s e r v a t i o n o f C a j a l z a n d L o r e n t e de N 6 ~ t h a t o c u l a r m o t o n e u r o n s are n o t p r o v i d e d w i t h r e c u r r e n t collaterals. Istituto di Fisiologia Umana dell'Universit& di Milano and lmpresa di Elettrofisiologia del CNR, Sezione di Milano, Milan (Italy)
FAUSTO BALDISSERA GIOVANNI BROGGI
I BACH-Y-RITA, P., AND MURATA, K., Extra-ocular proprioceptive receptors in VI nerve of cat, Quart. J. exp. Physiol., 49 (1964) 408-416. 2 CAJAL,S. RAM6N Y, Histologie du Systdme Nerveux de I'Homme et des Vertdbrds, Maloine, Paris, 1909, Vol. 1, XV, 986 pp. 3 DARIAN-SMITH, I., Presynaptic component in the afferent inhibition observed within trigeminal brain stem nuclei of the cat, J. Neurophysiol., 28 (1965) 695-709. 4 GASSER, H. S., AND ERLANGER, J., Electrical Signs o f Nervous Actions, Pennsylvania University Press, Philadelphia, 1937. 5 LORENTEDE NO, R., Action potentials of the motoneurons of the hypoglossus nucleus, J. cell. comp. Physiol., 29 (1947) 207-287. 6 McCoucH, G. P., AND ADLER, F. M., Extraocular reflexes, Amer. J. Physiol., 100 (1932) 78-88. 7 PALMIERI,G., AND ASOLE, A., On the presence of ganglion cells in the eye muscle nerves of some mammals and birds, Riv. Biol., 60 (1967) 139-152. 8 TOZER, F. M., AND SHERR~NGTON,C. S., Receptors and afferents of the third, fourth and sixth cranial nerves, Proc. roy. Soc. B., 82 (1910)450-457. (Accepted October 24th, 1967)
Brain Research, 7 (1968) 313-316