- Email: [email protected]
Cortical areas exerting presynaptic inhibitory action on the spinal cord in cat and monkey
SHORT COMMUNICATIONS
327
Cortical areas exerting presynaptic inhibitory action on the spinal cord in cat and monkey Stimulation of the sensorimotor cortex induces depression of transmission of the activity carried by ascending spinal tractsS, a. That this mechanism was presynaptic was demonstrated by Andersen et al. 1,~ and by Carpenter et al. a,4, who found dorsal root potentials (DRPs) when cortical areas SI and SII were stimulated. However, these authors explored only the convexity of the cortex and we felt that it would be interesting to study in addition the orbital cortex, which was shown by Korn et al. 7 to have afferent properties similar to those of the primary areas. We used 5 monkeys and 15 cats under chloralose anaesthesia (80 mg/kg i.v.) and 10 cats anaesthetized with pentobarbital (30 mg/kg i.v.). They were immobilized with gallamine and artificially ventilated. Body temperature, arterial pressure and alveolar CO2 were monitored continuously. After laminectomy the dura mater was opened and the cord exposed from L4 to S1. The D R P was recorded from a rootlet at the lumbar level. The root filament was mounted on electrodes and, together with the exposed cord, was covered with oil maintained at 37°C by a thermostatic heater. Amplifier time constant for D R P recording was 1 sec. The cortex was exposed; the orbital gyrus access was performed according to a previously described techniqueL First, we were able t o show that stimulation of the orbital cortex in cat under Nembutal (30 mg/kg i.v.) or chloralose (80 mg/kg i.v.) anaesthesia provokes DRPs.
CaL_NembuLal 30 mg//kg .i~/,
2",.. ] 1oo/~v
Cat_ChlorOose 80 mg/kg i.v.
Fig. 1. Cortical areas exerting presynaptic inhibitory action on the lumbar spinal cord in the cat. The size of the triangle is proportional to the amplitude of the DRP; no triangle has the significance of no effect. DRPs are recorded at L~. Brain Research, 20 (1970) 327-329
328
SHORT
Macacus Cynomolgus _ Chloralose 80 mg//kg
COMMUNICATIONS
i.,z
Fig. 2. Cortical areas exerting presynaptic inhibitory action on the lumbar spinal cord in the monkey. DRPs are recorded at Ls.
The surface area of the effective orbital zone is similar to that of SI and SII (Fig. 1) and the most effective region corresponds to the 'convergent orbital focus' of Korn et aLL Under chloralose anaesthesia, these areas become a little larger and, in particular, extend towards the motor cortex and visual and auditory primary areas (Fig. 1). The DRPs from the orbital cortex show characteristics of latency (25 msec for recording at L7) and duration similar to those from other areas and likewise require repetitive cortical stimulation (4-5 shocks at 200-300 c/sec) for their production. The regions studied induce bilateral DRPs. The predominant contralateral effect found in the pre- and postcruciate cortical areas 1 does not occur in the orbital gyrus or in SII. In the orbital cortex we found no somatotopic organization of the origin of the pathways; Andersen et al. ~ have already shown this for SII. Indeed our results on the pre- and postcruciate cortex differ in one point from those of Andersen et al.~: we have not found a strict somatotopic organization (especially under chloralose) but rather a 'preferential' type of organization. Working on the hypothesis that the degree of somatotopic organization of the DRPs' origin might depend upon the degree of neocortical development we carried out experiments on monkeys. In Macacus cynomolgus under chloralose anaesthesia, we found a strict somatotopy in the sensorimotor cortex (Fig. 2). The cortical points, which gave rise to DRPs at Ls, are distributed on either side of the central sulcus and spread over the medial surface of the hemisphere, extending all over the regions which receive afferents from the posterior limb. Stimulation of this posterior limb region does not produce primary afferent depolarization at the entrance level of forelimb afferents. However, stimulation of the cortical area of forelimb projection evoked P waves from the cord dorsum at the cervical level. Exploration of the area of vagal projection 9 and of the inferior surface of the frontal lobe was undertaken in the monkey in an attempt to define a region homologous to the cat orbital cortex, but with negative results. Brain Research, 20 (1970) 327-329
SHORT COMMUNICATIONS
329
In s u m m a r y , e x p l o r a t i o n o f the cat o r b i t a l c o r t e x has r e v e a l e d the existence o f an a r e a o f the s a m e size as SI a n d SII as j u d g e d b y the d e n s i t y o f the p o i n t s effective in p r o d u c i n g D R P s a n d b y the c o n s i d e r a b l e a m p l i t u d e o f the responses. These f e a t u r e s which the o r b i t a l cortex shares with SI a n d SII reinforce the evidence p r o d u c e d by several a u t h o r s that the o r b i t a l cortex should be c o n s i d e r e d as one o f the p r i m a r y cortical a r e a s 7. I n a d d i t i o n , the p r o d u c t i o n o f D R P s by s t i m u l a t i o n o f the o r b i t a l cortex suggests t h a t the i n h i b i t o r y effects which this a r e a exercises on certain limbs 10 or viscerom o t o r 0 reflexes m a y be m e d i a t e d by a m e c h a n i s m o f p r e s y n a p t i c inhibition. I n the case o f m o n k e y s , we have f o u n d evidence o f strict s o m a t o t o p i c o r g a n i z a t i o n o f the cortical areas which give rise to D R P s ; this fact is in o p p o s i t i o n to the p r e f e r e n t i a l o r g a n i z a t i o n o f the cortical areas e n c o u n t e r e d in cats. A n a r e a h o m o l ogous to o r b i t a l cortex in cat was n o t f o u n d in the m o n k e y .
Laboratoire de Physiologie des Centres Nerveux, 75 Paris 16e (France)
MOHAMMED ABDELMOUMI~NE JEAN-MARIE BESSON PIERRE ALI~ONARD
1 ANDERSEN,P., ECCLES,J. C., AND SEARS,T. A., Presynaptic inhibitory action of cerebral cortex on the spinal cord, Nature (Lond.), 194 (1962) 740-741. 2 ANDERSEN, P., ECCLES, J. C., AND SEARS, T. A., Cortically evoked depolarization of primary afferent fibers in the spinal cord, J. Neurophysiol., 27 (1964) 63-77. 3 CARPENTER,D., LUNDaERG,A., AND NORRSELL,U., Effects from the pyramidal tract on primary afferents and on spinal reflex actions to primary afferents, Experientia (Basel), 18 (1962) 337-338. 4 CARPENTER,O., LUNDaERG,A., AND NORRSELL,U., Primary afferent depolarization evoked from the sensorimotor cortex, Acta physiol, scand., 59 (1963) 126-142. 5 HAGBARTH,K. E., AND KERR, D. I. B., Central influences on spinal afferent conduction, J. Neurophysiol., 17 (1954) 295-307. 6 KORN, H., Control of the splanchno-intercostal reflex by orbital cortex in the cat, J. Physiol. (Lond.), 192 (1967) 33-34P. 7 KORN, H., WENDT, R., AND ALBE-FESSARD,D., Somatic projection to the orbital cortex of the cat, Electroenceph. clin. Neurophysiol., 21 (1966) 209-226. 8 MAGNI,F., AND OSCARSSON,O., Cerebral control of transmission to the ventral spinocerebellar tract, Arch. ital. Biol., 99 (1961) 369-396. 9 PIMPANEAU,A., O'BRIEN, J., ET ALaE-FESSARD,D., Aff6rences du neff laryng6 sup6rieur et du nerf vague vers les aires corticales de projection et de commande de la face, de la langue et du larynx chez le singe, J. Physiol. (Paris), 59 (1967) 474. 10 SAUERLAND,E. K., KNAUSS,T., NAKAMURA,Y., AND CLEMENTE,C. D., Inhibition ofmonosynaptic and polysynaptic reflexes and muscle tone by electrical stimulation of the cerebral cortex, Exp. Neurol., 17 (1967) 159-172.
(Accepted March 24th, 1970)
Brain Research, 20 (1970) 327-329
327
Cortical areas exerting presynaptic inhibitory action on the spinal cord in cat and monkey Stimulation of the sensorimotor cortex induces depression of transmission of the activity carried by ascending spinal tractsS, a. That this mechanism was presynaptic was demonstrated by Andersen et al. 1,~ and by Carpenter et al. a,4, who found dorsal root potentials (DRPs) when cortical areas SI and SII were stimulated. However, these authors explored only the convexity of the cortex and we felt that it would be interesting to study in addition the orbital cortex, which was shown by Korn et al. 7 to have afferent properties similar to those of the primary areas. We used 5 monkeys and 15 cats under chloralose anaesthesia (80 mg/kg i.v.) and 10 cats anaesthetized with pentobarbital (30 mg/kg i.v.). They were immobilized with gallamine and artificially ventilated. Body temperature, arterial pressure and alveolar CO2 were monitored continuously. After laminectomy the dura mater was opened and the cord exposed from L4 to S1. The D R P was recorded from a rootlet at the lumbar level. The root filament was mounted on electrodes and, together with the exposed cord, was covered with oil maintained at 37°C by a thermostatic heater. Amplifier time constant for D R P recording was 1 sec. The cortex was exposed; the orbital gyrus access was performed according to a previously described techniqueL First, we were able t o show that stimulation of the orbital cortex in cat under Nembutal (30 mg/kg i.v.) or chloralose (80 mg/kg i.v.) anaesthesia provokes DRPs.
CaL_NembuLal 30 mg//kg .i~/,
2",.. ] 1oo/~v
Cat_ChlorOose 80 mg/kg i.v.
Fig. 1. Cortical areas exerting presynaptic inhibitory action on the lumbar spinal cord in the cat. The size of the triangle is proportional to the amplitude of the DRP; no triangle has the significance of no effect. DRPs are recorded at L~. Brain Research, 20 (1970) 327-329
328
SHORT
Macacus Cynomolgus _ Chloralose 80 mg//kg
COMMUNICATIONS
i.,z
Fig. 2. Cortical areas exerting presynaptic inhibitory action on the lumbar spinal cord in the monkey. DRPs are recorded at Ls.
The surface area of the effective orbital zone is similar to that of SI and SII (Fig. 1) and the most effective region corresponds to the 'convergent orbital focus' of Korn et aLL Under chloralose anaesthesia, these areas become a little larger and, in particular, extend towards the motor cortex and visual and auditory primary areas (Fig. 1). The DRPs from the orbital cortex show characteristics of latency (25 msec for recording at L7) and duration similar to those from other areas and likewise require repetitive cortical stimulation (4-5 shocks at 200-300 c/sec) for their production. The regions studied induce bilateral DRPs. The predominant contralateral effect found in the pre- and postcruciate cortical areas 1 does not occur in the orbital gyrus or in SII. In the orbital cortex we found no somatotopic organization of the origin of the pathways; Andersen et al. ~ have already shown this for SII. Indeed our results on the pre- and postcruciate cortex differ in one point from those of Andersen et al.~: we have not found a strict somatotopic organization (especially under chloralose) but rather a 'preferential' type of organization. Working on the hypothesis that the degree of somatotopic organization of the DRPs' origin might depend upon the degree of neocortical development we carried out experiments on monkeys. In Macacus cynomolgus under chloralose anaesthesia, we found a strict somatotopy in the sensorimotor cortex (Fig. 2). The cortical points, which gave rise to DRPs at Ls, are distributed on either side of the central sulcus and spread over the medial surface of the hemisphere, extending all over the regions which receive afferents from the posterior limb. Stimulation of this posterior limb region does not produce primary afferent depolarization at the entrance level of forelimb afferents. However, stimulation of the cortical area of forelimb projection evoked P waves from the cord dorsum at the cervical level. Exploration of the area of vagal projection 9 and of the inferior surface of the frontal lobe was undertaken in the monkey in an attempt to define a region homologous to the cat orbital cortex, but with negative results. Brain Research, 20 (1970) 327-329
SHORT COMMUNICATIONS
329
In s u m m a r y , e x p l o r a t i o n o f the cat o r b i t a l c o r t e x has r e v e a l e d the existence o f an a r e a o f the s a m e size as SI a n d SII as j u d g e d b y the d e n s i t y o f the p o i n t s effective in p r o d u c i n g D R P s a n d b y the c o n s i d e r a b l e a m p l i t u d e o f the responses. These f e a t u r e s which the o r b i t a l cortex shares with SI a n d SII reinforce the evidence p r o d u c e d by several a u t h o r s that the o r b i t a l cortex should be c o n s i d e r e d as one o f the p r i m a r y cortical a r e a s 7. I n a d d i t i o n , the p r o d u c t i o n o f D R P s by s t i m u l a t i o n o f the o r b i t a l cortex suggests t h a t the i n h i b i t o r y effects which this a r e a exercises on certain limbs 10 or viscerom o t o r 0 reflexes m a y be m e d i a t e d by a m e c h a n i s m o f p r e s y n a p t i c inhibition. I n the case o f m o n k e y s , we have f o u n d evidence o f strict s o m a t o t o p i c o r g a n i z a t i o n o f the cortical areas which give rise to D R P s ; this fact is in o p p o s i t i o n to the p r e f e r e n t i a l o r g a n i z a t i o n o f the cortical areas e n c o u n t e r e d in cats. A n a r e a h o m o l ogous to o r b i t a l cortex in cat was n o t f o u n d in the m o n k e y .
Laboratoire de Physiologie des Centres Nerveux, 75 Paris 16e (France)
MOHAMMED ABDELMOUMI~NE JEAN-MARIE BESSON PIERRE ALI~ONARD
1 ANDERSEN,P., ECCLES,J. C., AND SEARS,T. A., Presynaptic inhibitory action of cerebral cortex on the spinal cord, Nature (Lond.), 194 (1962) 740-741. 2 ANDERSEN, P., ECCLES, J. C., AND SEARS, T. A., Cortically evoked depolarization of primary afferent fibers in the spinal cord, J. Neurophysiol., 27 (1964) 63-77. 3 CARPENTER,D., LUNDaERG,A., AND NORRSELL,U., Effects from the pyramidal tract on primary afferents and on spinal reflex actions to primary afferents, Experientia (Basel), 18 (1962) 337-338. 4 CARPENTER,O., LUNDaERG,A., AND NORRSELL,U., Primary afferent depolarization evoked from the sensorimotor cortex, Acta physiol, scand., 59 (1963) 126-142. 5 HAGBARTH,K. E., AND KERR, D. I. B., Central influences on spinal afferent conduction, J. Neurophysiol., 17 (1954) 295-307. 6 KORN, H., Control of the splanchno-intercostal reflex by orbital cortex in the cat, J. Physiol. (Lond.), 192 (1967) 33-34P. 7 KORN, H., WENDT, R., AND ALBE-FESSARD,D., Somatic projection to the orbital cortex of the cat, Electroenceph. clin. Neurophysiol., 21 (1966) 209-226. 8 MAGNI,F., AND OSCARSSON,O., Cerebral control of transmission to the ventral spinocerebellar tract, Arch. ital. Biol., 99 (1961) 369-396. 9 PIMPANEAU,A., O'BRIEN, J., ET ALaE-FESSARD,D., Aff6rences du neff laryng6 sup6rieur et du nerf vague vers les aires corticales de projection et de commande de la face, de la langue et du larynx chez le singe, J. Physiol. (Paris), 59 (1967) 474. 10 SAUERLAND,E. K., KNAUSS,T., NAKAMURA,Y., AND CLEMENTE,C. D., Inhibition ofmonosynaptic and polysynaptic reflexes and muscle tone by electrical stimulation of the cerebral cortex, Exp. Neurol., 17 (1967) 159-172.
(Accepted March 24th, 1970)
Brain Research, 20 (1970) 327-329