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Somatic sensory properties of red nucleus neurons
264
SHORT ('OMMUNICATIONS
W e are grateful to Dr. Hiroshi Shimazu, Brain Research Institute o f the University o f T o k y o . T h r o u g h a discussion with him, we were led to the p r o b l e m treated in this paper. Department of Neurophysiology, Institute of Higher Nervous Activity, Osaka University Medical School, Kita-ku, Osaka (Japan)
ICHIJI SUMITOMO KEIZO I DE KITSUYA IWAMA
1 ARIKUNI, T., AND IWAMA, K., Functional changes in optic tract fibers and lateral geniculate neurons following chronic ablation of visual cortex in rats, Med. J. Osaka Univ., 17 (1967) 223-236. 2 BISHOP, G. H., AND CLARE, m., Sequence of events in optic cortex response to volleys of impulses in the radiation, J. Neurophysiol., 16 (1953) 490-498. 3 BISHOP, P. O., AND EVANS, W. A., The refractory period of the sensory synapses of the lateral geniculate nucleus, J. Physiol. (Lond.), 134 (1956) 538-557. 4 BURKE, W., AND SEFTON, A. J., Discharge patterns of principal cells and interneurons in lateral geniculate nucleus of rat, J. Physiol. (Lond.), 187 (1966) 201-212. 5 NODA, H., AND IWAMA, K., Unitary analysis of retino-geniculate response time in rats, Vision Res., 7 (1967) 205-213. 6 SEFTON, A. J., AND SWINBURN, M., Electrical activity of lateral geniculate nucleus and optic tract of the rat, Vision Res., 4 (1964) 315-328. 7 SUMITOMO,I., AND IWAMA,K., Discharge frequency of the lateral geniculate neurons as a function of response latency to optic tract stimulation, Brain Research, 6 (1967) 395-397. (Accepted October 5th, 1968) Brain Research, 12 (1969) 261-264
Somatic sensory properties of red nucleus neurons There exists a considerable a m o u n t o f literature on the somatic sensory afferents to the m a g n o c e l l u l a r p a r t o f the red nucleus ( R N ) neurons 2,3, b u t we have, as yet, little i n f o r m a t i o n as to w h a t is involved in the m o d a l i t y o f somatic sensory stimulus activating the R N neurons a n d their s o m a t o t o p i c organization. The present study was designed to secure this i n f o r m a t i o n . Experiments were p e r f o r m e d on 12 cats. Ether was used for the o p e r a t i o n . The trachea was c a n n u l a t e d a n d a venous c a n n u l a was inserted into a superficial hind limb vein, all operative w o u n d s were carefully closed, and the a n i m a l ' s head was fixed on a stereotaxic instrument. The skull was t r e p h i n e d over R N . W o u n d m a r g i n s and pressure p o i n t s were infiltrated with 2 ~ procaine. The animals were finally i m m o b i l i z e d with gallamine triethiodide a n d m a i n t a i n e d u n d e r artificial respiration. The impulse activity from a single n e u r o n was r e c o r d e d with stainless steel microelectrodes I a n d amplified in a c o n v e n t i o n a l manner. E l e c t r o e n c e p h a l o g r a p h i c recordings were also m a d e f r o m the somatic sensory area o f the cerebral cortex. These recordings suggested t h a t the a n i m a l was usually in a state o f light sleep if he was k e p t quiet. T o determine the site a n d size o f the receptive fields a n d the response properties o f individual neurons, n a t u r a l stimuli were offered such as b e n d i n g hairs with an air-puff or with small brushes, touching the skin lightly with a glass rod, as well as pressing it with a w o o d e n stick. Joints were r o t a t e d by hand. A n i m a l s were Brain Research, 12 (1969) 264-267
SHORT COMMUNICATIONS
265
Fig. 1. Data obtained in the dorso-ventral penetration of a microelectrode passed through RN in the left side of the midbrain. The penetration is reconstructed in the drawing at the left. Lines connecting the drawing at the right to the vertical line give the positions along the penetration where the neurons were isolated. The scale to the left ." 1 mm. The receptive fields of the neurons are shown to the right. Areas from which hair movements excite the activity of the neurons are indicated by oblique lines and higher sensitivities with hair movements are shown by crossed lines. Horizontal lines indicate an area from which light mechanical stimuli delivered to the skin inhibit the activity of the neurons (I). A indicated near the right drawing shows the neurons activated by sound as well as by hair movements. CG: central grey matter, SN: substantia nigra, PED: cerebral peduncle, Ill: third nerve.
also t a p p e d on the superficial a n d deep tissues. In some neurons, stimuli considered to be n o x i o u s were given by p i n c h i n g the skin with t o o t h e d forceps. N o n - s o m a t i c stimuli consisted o f light flashes, sudden p r e s e n t a t i o n o f light over the a n i m a l ' s eye; claps or tones were also given. A t the end o f an experiment, currents o f 10 # A were passed t h r o u g h each needle electrode for 20 sec to m a r k the p o s i t i o n o f the electrode tip. A f t e r the a n i m a l s were sacrificed by i.v. injection o f p e n t o b a r b i t o n e sodium, 1 0 ~ f o r m a l i n with a b o u t 2700 p o t a s s i u m f e r r o c y a n i d e a d d e d was injected into the c a r o t i d artery for fixation o f the brain. F r o n t a l serial frozen sections o f 25 # thickness were stained with 0.2 700 cresyl violet, a n d the a p p r o x i m a t e r e c o r d i n g sites were determined. T h e present results are based on the evidence o b t a i n e d f r o m the 87 R N neurons, all o f which r e s p o n d e d to the n a t u r a l stimuli. A s the electrode traversed R N dorsally to ventrally, the receptive fields g r a d u a l l y m o v e d f r o m the u p p e r h a l f to the lower h a l f o f the b o d y (Fig. 1). I n m o s t cases, the first n e u r o n s e n c o u n t e r e d d u r i n g the p e n e t r a t i o n s were sensitive only to s t i m u l a t i o n o f the face (Fig. 2A). The d o r s a l Brain Research, 12 (1969) 264-267
266
SHORT COMMUNICATIONS
A
C
D
E-
E
B
Fig. 2. A representative sample of the receptive fields of the RN neurons. Oblique lines indicate an area from which the neurons respond to hair bending; horizontal lines, to light mechanical stimuli applied to the skin; black, to tapping; dots, to nociceptive stimuli. Crossed lines indicate higher sensitivities with hair movement. Two neurons are responsive with joint rotation of which the direction is shown by arrows. E: excitatory receptive field. I : inhibitory receptive field. The contralateral side of the body is shown to the right of the drawings. region of R N receives the afferent inputs from the face and the upper half of the body, and the ventral region from the lower half of the body; there is some overlapping between the receiving areas of RN. This somatotopical pattern corresponds well with that of the origin of the rubrospinal projection 5,7. Out of 87 neurons, 54 were responsive to gentle displacement of hairs; 27, not to hair bending but to light mechanical stimuli to the skin; 6, only to stimulation applied to the deep tissues. Out of 54 neurons responsive to hair movement, 18 also responded to stimulation of the deep tissues. Out of 27 neurons driven by light mechanical stimuli to the skin, 17 also responded to stimulation of the deep tissues. The receptive fields of the skin and of the deep tissues were not widely separated on the body, but were located near each other (Fig. 2B). Some neurons were sensitive to both somatic and auditory stimuli (2 out of 21 neurons examined), and some to both somatic and visual stimuli (2 out of 12 neurons). Excitatory and inhibitory effects were found in the R N neurons (17 out of 87 neurons), and inhibitory fields were usually located near excitatory fields (Fig. 2C). Out of 87 neurons, 23 responded with rapid adaptation to joint rotation, and their firing pattern was different from that in the ventrobasal complex of the thalamus 4. Out of 7 neurons studied in detail with noxious stimuli, 3 were responsive to pinching the skin with toothed forceps, but not with non-toothed forceps. They also Brain Research, 12 (1969) 264-267
SHORT COMMUNICATIONS
267
responded to hair bending, and to stimulation of the deep tissues (Fig. 2D). When the skin was pinched with toothed forceps for 5 sec, the nociceptive neurons of R N rapidly responded with high-frequency discharges which subsided to a rate of spontaneous activity about 2 sec after the stimulation. This firing pattern differs from that of the nociceptive neurons of the posterior group of the thalamus, which showed a slow increase of discharges and prolonged after-discharges after removal of the noxious stimuli 6. Massion and Albe-Fessard a showed in chloralose-treated cats that the RN neurons did not respond to hair bending. However, this study indicates in immobilized and locally anesthetized cats that not only hair bending but nociceptive stimuli elicit the responses of the R N neurons. The following conclusions may be drawn: (1) the R N neurons receive somatic sensory inputs with somatotopical pattern; (2) effective stimuli to drive the R N neurons are hair bending, light mechanical stimuli to the skin, tapping on the superficial and the deep tissues, joint rotation, and nociceptive stimuli; (3) relatively many R N neurons are polyvalent with respect to such different somatic stimuli. We express our appreciation to Dr. Morinaga Ueda for his constant advice and encouragement and to Miss Yukie Arai for her skilful technical assistance. Dr Toshio Kusama and Dr. Masako Mabuchi provided valuable suggestions in this study. Division of Neurophysiology, Institute of Brain Diseases, Tohoku University School of Medicine, Sendai, and Neurophysiology Section, The Seishin-lgaku Institute, Itabashi-ku, Tokyo (Japan)
HIROSHI NAKAHAMA SADAO AIKAWA SHINKO NISHIOKA
1 GREEN,J. D., A simple microelectrode for recording from the central nervous system, Nature (Lond.), 182 (1958) 962. 2 MASSION,J., The mammalian red nucleus, Physiol. Rev., 47 (1967) 383-436. 3 MASSION,J., ET ALBE-FESSARD,D., Dualit6 des voies sensorielles aff6rentes contr61ant l'activit6 du noyau rouge, Electroenceph. clin. Neurophysiol., 15 (1963) 435-454. 4 MOUNTCASTLE, V. B., POGGtO,G. F., AND WERNER, G., The relation of thalamic cell response to peripheral stimuli varied over an intensive continuum, J. Neurophysiol., 26 (1963) 807-834. 5 NYBERG-HANSEN, R., AND BRODAL, A., Site and mode of termination of rubro-spinal fibres in the cat. An experimental study with silver impregnation methods, J. Anat. (Lond.), 98 (1964) 235-253. 6 POGGIO,G. F., aND MOUNTCASTLE,V. B., A study of the functional contributions of the lemniscal and spinothalamic systems to somatic sensibility. Central nervous mechanisms in pain, Bull. Johns Hopk. Hosp., 106 (1960) 266-316. 7 laOMPEIANO,O., ANDBRODAL,A., Experimental demonstration of a somatotopical origin of rubrospinal fibres in the cat, J. comp. Neurol., 108 (1957) 225-252. (Accepted October 17th, 1968)
Brain Research, 12 (1969) 264-267
SHORT ('OMMUNICATIONS
W e are grateful to Dr. Hiroshi Shimazu, Brain Research Institute o f the University o f T o k y o . T h r o u g h a discussion with him, we were led to the p r o b l e m treated in this paper. Department of Neurophysiology, Institute of Higher Nervous Activity, Osaka University Medical School, Kita-ku, Osaka (Japan)
ICHIJI SUMITOMO KEIZO I DE KITSUYA IWAMA
1 ARIKUNI, T., AND IWAMA, K., Functional changes in optic tract fibers and lateral geniculate neurons following chronic ablation of visual cortex in rats, Med. J. Osaka Univ., 17 (1967) 223-236. 2 BISHOP, G. H., AND CLARE, m., Sequence of events in optic cortex response to volleys of impulses in the radiation, J. Neurophysiol., 16 (1953) 490-498. 3 BISHOP, P. O., AND EVANS, W. A., The refractory period of the sensory synapses of the lateral geniculate nucleus, J. Physiol. (Lond.), 134 (1956) 538-557. 4 BURKE, W., AND SEFTON, A. J., Discharge patterns of principal cells and interneurons in lateral geniculate nucleus of rat, J. Physiol. (Lond.), 187 (1966) 201-212. 5 NODA, H., AND IWAMA, K., Unitary analysis of retino-geniculate response time in rats, Vision Res., 7 (1967) 205-213. 6 SEFTON, A. J., AND SWINBURN, M., Electrical activity of lateral geniculate nucleus and optic tract of the rat, Vision Res., 4 (1964) 315-328. 7 SUMITOMO,I., AND IWAMA,K., Discharge frequency of the lateral geniculate neurons as a function of response latency to optic tract stimulation, Brain Research, 6 (1967) 395-397. (Accepted October 5th, 1968) Brain Research, 12 (1969) 261-264
Somatic sensory properties of red nucleus neurons There exists a considerable a m o u n t o f literature on the somatic sensory afferents to the m a g n o c e l l u l a r p a r t o f the red nucleus ( R N ) neurons 2,3, b u t we have, as yet, little i n f o r m a t i o n as to w h a t is involved in the m o d a l i t y o f somatic sensory stimulus activating the R N neurons a n d their s o m a t o t o p i c organization. The present study was designed to secure this i n f o r m a t i o n . Experiments were p e r f o r m e d on 12 cats. Ether was used for the o p e r a t i o n . The trachea was c a n n u l a t e d a n d a venous c a n n u l a was inserted into a superficial hind limb vein, all operative w o u n d s were carefully closed, and the a n i m a l ' s head was fixed on a stereotaxic instrument. The skull was t r e p h i n e d over R N . W o u n d m a r g i n s and pressure p o i n t s were infiltrated with 2 ~ procaine. The animals were finally i m m o b i l i z e d with gallamine triethiodide a n d m a i n t a i n e d u n d e r artificial respiration. The impulse activity from a single n e u r o n was r e c o r d e d with stainless steel microelectrodes I a n d amplified in a c o n v e n t i o n a l manner. E l e c t r o e n c e p h a l o g r a p h i c recordings were also m a d e f r o m the somatic sensory area o f the cerebral cortex. These recordings suggested t h a t the a n i m a l was usually in a state o f light sleep if he was k e p t quiet. T o determine the site a n d size o f the receptive fields a n d the response properties o f individual neurons, n a t u r a l stimuli were offered such as b e n d i n g hairs with an air-puff or with small brushes, touching the skin lightly with a glass rod, as well as pressing it with a w o o d e n stick. Joints were r o t a t e d by hand. A n i m a l s were Brain Research, 12 (1969) 264-267
SHORT COMMUNICATIONS
265
Fig. 1. Data obtained in the dorso-ventral penetration of a microelectrode passed through RN in the left side of the midbrain. The penetration is reconstructed in the drawing at the left. Lines connecting the drawing at the right to the vertical line give the positions along the penetration where the neurons were isolated. The scale to the left ." 1 mm. The receptive fields of the neurons are shown to the right. Areas from which hair movements excite the activity of the neurons are indicated by oblique lines and higher sensitivities with hair movements are shown by crossed lines. Horizontal lines indicate an area from which light mechanical stimuli delivered to the skin inhibit the activity of the neurons (I). A indicated near the right drawing shows the neurons activated by sound as well as by hair movements. CG: central grey matter, SN: substantia nigra, PED: cerebral peduncle, Ill: third nerve.
also t a p p e d on the superficial a n d deep tissues. In some neurons, stimuli considered to be n o x i o u s were given by p i n c h i n g the skin with t o o t h e d forceps. N o n - s o m a t i c stimuli consisted o f light flashes, sudden p r e s e n t a t i o n o f light over the a n i m a l ' s eye; claps or tones were also given. A t the end o f an experiment, currents o f 10 # A were passed t h r o u g h each needle electrode for 20 sec to m a r k the p o s i t i o n o f the electrode tip. A f t e r the a n i m a l s were sacrificed by i.v. injection o f p e n t o b a r b i t o n e sodium, 1 0 ~ f o r m a l i n with a b o u t 2700 p o t a s s i u m f e r r o c y a n i d e a d d e d was injected into the c a r o t i d artery for fixation o f the brain. F r o n t a l serial frozen sections o f 25 # thickness were stained with 0.2 700 cresyl violet, a n d the a p p r o x i m a t e r e c o r d i n g sites were determined. T h e present results are based on the evidence o b t a i n e d f r o m the 87 R N neurons, all o f which r e s p o n d e d to the n a t u r a l stimuli. A s the electrode traversed R N dorsally to ventrally, the receptive fields g r a d u a l l y m o v e d f r o m the u p p e r h a l f to the lower h a l f o f the b o d y (Fig. 1). I n m o s t cases, the first n e u r o n s e n c o u n t e r e d d u r i n g the p e n e t r a t i o n s were sensitive only to s t i m u l a t i o n o f the face (Fig. 2A). The d o r s a l Brain Research, 12 (1969) 264-267
266
SHORT COMMUNICATIONS
A
C
D
E-
E
B
Fig. 2. A representative sample of the receptive fields of the RN neurons. Oblique lines indicate an area from which the neurons respond to hair bending; horizontal lines, to light mechanical stimuli applied to the skin; black, to tapping; dots, to nociceptive stimuli. Crossed lines indicate higher sensitivities with hair movement. Two neurons are responsive with joint rotation of which the direction is shown by arrows. E: excitatory receptive field. I : inhibitory receptive field. The contralateral side of the body is shown to the right of the drawings. region of R N receives the afferent inputs from the face and the upper half of the body, and the ventral region from the lower half of the body; there is some overlapping between the receiving areas of RN. This somatotopical pattern corresponds well with that of the origin of the rubrospinal projection 5,7. Out of 87 neurons, 54 were responsive to gentle displacement of hairs; 27, not to hair bending but to light mechanical stimuli to the skin; 6, only to stimulation applied to the deep tissues. Out of 54 neurons responsive to hair movement, 18 also responded to stimulation of the deep tissues. Out of 27 neurons driven by light mechanical stimuli to the skin, 17 also responded to stimulation of the deep tissues. The receptive fields of the skin and of the deep tissues were not widely separated on the body, but were located near each other (Fig. 2B). Some neurons were sensitive to both somatic and auditory stimuli (2 out of 21 neurons examined), and some to both somatic and visual stimuli (2 out of 12 neurons). Excitatory and inhibitory effects were found in the R N neurons (17 out of 87 neurons), and inhibitory fields were usually located near excitatory fields (Fig. 2C). Out of 87 neurons, 23 responded with rapid adaptation to joint rotation, and their firing pattern was different from that in the ventrobasal complex of the thalamus 4. Out of 7 neurons studied in detail with noxious stimuli, 3 were responsive to pinching the skin with toothed forceps, but not with non-toothed forceps. They also Brain Research, 12 (1969) 264-267
SHORT COMMUNICATIONS
267
responded to hair bending, and to stimulation of the deep tissues (Fig. 2D). When the skin was pinched with toothed forceps for 5 sec, the nociceptive neurons of R N rapidly responded with high-frequency discharges which subsided to a rate of spontaneous activity about 2 sec after the stimulation. This firing pattern differs from that of the nociceptive neurons of the posterior group of the thalamus, which showed a slow increase of discharges and prolonged after-discharges after removal of the noxious stimuli 6. Massion and Albe-Fessard a showed in chloralose-treated cats that the RN neurons did not respond to hair bending. However, this study indicates in immobilized and locally anesthetized cats that not only hair bending but nociceptive stimuli elicit the responses of the R N neurons. The following conclusions may be drawn: (1) the R N neurons receive somatic sensory inputs with somatotopical pattern; (2) effective stimuli to drive the R N neurons are hair bending, light mechanical stimuli to the skin, tapping on the superficial and the deep tissues, joint rotation, and nociceptive stimuli; (3) relatively many R N neurons are polyvalent with respect to such different somatic stimuli. We express our appreciation to Dr. Morinaga Ueda for his constant advice and encouragement and to Miss Yukie Arai for her skilful technical assistance. Dr Toshio Kusama and Dr. Masako Mabuchi provided valuable suggestions in this study. Division of Neurophysiology, Institute of Brain Diseases, Tohoku University School of Medicine, Sendai, and Neurophysiology Section, The Seishin-lgaku Institute, Itabashi-ku, Tokyo (Japan)
HIROSHI NAKAHAMA SADAO AIKAWA SHINKO NISHIOKA
1 GREEN,J. D., A simple microelectrode for recording from the central nervous system, Nature (Lond.), 182 (1958) 962. 2 MASSION,J., The mammalian red nucleus, Physiol. Rev., 47 (1967) 383-436. 3 MASSION,J., ET ALBE-FESSARD,D., Dualit6 des voies sensorielles aff6rentes contr61ant l'activit6 du noyau rouge, Electroenceph. clin. Neurophysiol., 15 (1963) 435-454. 4 MOUNTCASTLE, V. B., POGGtO,G. F., AND WERNER, G., The relation of thalamic cell response to peripheral stimuli varied over an intensive continuum, J. Neurophysiol., 26 (1963) 807-834. 5 NYBERG-HANSEN, R., AND BRODAL, A., Site and mode of termination of rubro-spinal fibres in the cat. An experimental study with silver impregnation methods, J. Anat. (Lond.), 98 (1964) 235-253. 6 POGGIO,G. F., aND MOUNTCASTLE,V. B., A study of the functional contributions of the lemniscal and spinothalamic systems to somatic sensibility. Central nervous mechanisms in pain, Bull. Johns Hopk. Hosp., 106 (1960) 266-316. 7 laOMPEIANO,O., ANDBRODAL,A., Experimental demonstration of a somatotopical origin of rubrospinal fibres in the cat, J. comp. Neurol., 108 (1957) 225-252. (Accepted October 17th, 1968)
Brain Research, 12 (1969) 264-267