Brain Research, 507 (1990) 337-340
337
Elsevier BRES 23922
Input-output relationships in the jaw and orofacial motor zones of the cat cerebral cortex Koichi Iwata, Hiroyuki Muramatsu, Yoshiyuki Tsuboi and Rhyuji Sumino Department of Physiology, School of Dentistry, Nihon University, Tokyo (Japan) (Accepted 3 October 1989)
Key words: Motor effect: Intracortical microstimulation; Jaw and orofacial motor zones; Input-output relationship; Cerebral cortex;
Cat
Input-output relationships of the jaw and orofacial motor zones in the cerebral cortex of lightly anesthetized cats were studied. These relationships were examined by studying the motor effects produced by intracortical microstimulation (ICMS) and recording from single neuron. Jaw and orofacial motor effects were evoked by ICMS of the anterior part of the coronal and lateral sigmoid gyri (C-S motor zone) and the lateral wall of the presylvian sulcus (P motor zone). ICMS of the P motor zone produced more complex movements than that of the C-S motor zone. Repetitive stimulation of the P motor zone also evoked rhythmic jaw movements. Almost all cortical ceils located in the C-S motor zone responded to tactile stimulation of cutaneous skin of the orofacial regions or the tooth, whereas those of the P motor zone received no cutaneous input from the orofacial regions. Cytoarchitectonically, the C-S motor zone was restricted to areas 3a, 6aft and occasionally to area 4V, whereas the P motor zone was represented to area 6aft. Therefore, it is concluded that the C-S motor zone might be involved in sensorimotor integration of the jaw and orofacial motor functions, whereas the P motor zone might function only as a command area for jaw and orofacial movements. M o v e m e n t s of the jaw and orofacial regions occur after electrical stimulation of two separate regions of the c a t cerebral cortex: the anterior part of the coronal and lateral sigmoid gyri and the anterior part of the orbital gyrus3,4,6,7.s. ~(~.11.14,15,22,23. Electrical stimulation of a r e a s 3a and 3b of the anterior part of the coronal gyrus also efficiently m o d u l a t e s the monosynaptic jaw closing and the disynaptic jaw o p e n i n g reflex t6"~7. However, stimulation of the perioral projection areas, 5a (anterior suprasylvian gyrus), 6aft (presylvian gyrus) and 43 (orbital gyrus), p r o d u c e s smaller effects mainly consisting of inhibition. These observations suggest that the axons of neurons located in the anterior part of the coronal and lateral sigmoid gyri project to the brainstem. In a m o r p h o l o g i c a l study, Yasui et al. ~4 confirmed that neurons located in the anterior part of the coronal and lateral sigmoid gyri p r o j e c t e d to the region of the trigeminal m o t o r nucleus and d e m o n s t r a t e d that fibers also projected directly to the brainstem from the lateral wall of the presylvian sulcus. This suggests that the lateral wall of the presylvian sulcus may function as the jaw and orofacial m o t o r cortex. Therefore, 3 separate jaw and orofacial m o t o r zones have been d e m o n s t r a t e d in the frontal cortex of cats: the coronal and lateral sigmoid gyri, the lateral wall of the suprasylvian sulcus, and the anterior part of the orbital gyrus. Landgren and Olsson '> studied the cortical p r o j e c t i o n of trigeminal afferents and showed that low-threshold trigeminal afferents p r o j e c t e d
to overlapping somatotopically organized fields in a r e a s 3a and 3b of the anterior coronal gyrus, to a r e a 6aft of the presylvian and anterior coronal gyrus, and to area 5a of the anterior suprasylvian gyrus. M o r e recently, Taira 2°'2~ r e p o r t e d a s o m a t o t o p i c r e p r e s e n t a t i o n of the intraoral structures in the anterior part of the coronal gyrus. These results suggest that the anterior part of the coronal and lateral sigmoid gyri and the lateral wall of the presylvian sulcus are related to the m o t o r function of the jaw and orofacial regions which is controlled by the non-noxious cutaneous sensory information from jaw and orofacial regions, The present study e x a m i n e d the cortical s e n s o r i m o t o r integration of jaw and orofacial regions in which both sensory input and ICMS were investigated at the same loci. A d d i t i o n a l l y , this study described spatial organization of i n p u t - o u t p u t coupling in the orofacial m o t o r zone of the anterior part of the coronal, the lateral sigmoid gyri and the lateral wall of the presylvian sulcus. E x p e r i m e n t s were p e r f o r m e d on 13 adult cats (2.5-3.5 kg) anesthetized with k e t a m i n e HC1 (initial dose of about 50 mg/kg, i.m.). The skull was o p e n e d over the coronal and lateral sigmoid gyri and a d j a c e n t regions, and the left eye ball was removed. A n acrylic c h a m b e r was placed over the skull opening and filled with mineral oil. The head was rigidly secured to a frame by means of s t a i n l e s s steel screws attached to the skull and e m b e d d e d in dental acrylic cement. Each animal was m a i n t a i n e d in a sedated
Correspondence: K. Iwata. Department of Physiology, School of Dentislry, Nikon University, 1-8-13 Kandasurugadai, Chiyoda-ku, Tokyo 101, Japan. 0006-8993/90/$(13.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
338 state throughout the experiment by continuous intramuscular infusion of ketamine HC1 (10 mg/kg/1 h). Sedative level was judged by miosis and animal's movement. When the animal's pupil quickly responded to light presentation or animals made gross non-reflexive movement, additional ketamine HCI (10 mg/kg) was injected i.m. The traumatized tissues were infiltrated with 2% lidocaine-HC1 solution in order to prevent postsurgical pain during the experiment. Tungsten-in-glass microelectrodes were inserted into the coronal and lateral sigmoid gyri and the lateral wall of the presylvian sulcus to record unitary activities as well as to deliver ICMS. The electrodes were advanced through the cortex in 200 ltm steps. At each step, ICMS (0.2 ms, 12 cathodal pulses;
337
Elsevier BRES 23922
Input-output relationships in the jaw and orofacial motor zones of the cat cerebral cortex Koichi Iwata, Hiroyuki Muramatsu, Yoshiyuki Tsuboi and Rhyuji Sumino Department of Physiology, School of Dentistry, Nihon University, Tokyo (Japan) (Accepted 3 October 1989)
Key words: Motor effect: Intracortical microstimulation; Jaw and orofacial motor zones; Input-output relationship; Cerebral cortex;
Cat
Input-output relationships of the jaw and orofacial motor zones in the cerebral cortex of lightly anesthetized cats were studied. These relationships were examined by studying the motor effects produced by intracortical microstimulation (ICMS) and recording from single neuron. Jaw and orofacial motor effects were evoked by ICMS of the anterior part of the coronal and lateral sigmoid gyri (C-S motor zone) and the lateral wall of the presylvian sulcus (P motor zone). ICMS of the P motor zone produced more complex movements than that of the C-S motor zone. Repetitive stimulation of the P motor zone also evoked rhythmic jaw movements. Almost all cortical ceils located in the C-S motor zone responded to tactile stimulation of cutaneous skin of the orofacial regions or the tooth, whereas those of the P motor zone received no cutaneous input from the orofacial regions. Cytoarchitectonically, the C-S motor zone was restricted to areas 3a, 6aft and occasionally to area 4V, whereas the P motor zone was represented to area 6aft. Therefore, it is concluded that the C-S motor zone might be involved in sensorimotor integration of the jaw and orofacial motor functions, whereas the P motor zone might function only as a command area for jaw and orofacial movements. M o v e m e n t s of the jaw and orofacial regions occur after electrical stimulation of two separate regions of the c a t cerebral cortex: the anterior part of the coronal and lateral sigmoid gyri and the anterior part of the orbital gyrus3,4,6,7.s. ~(~.11.14,15,22,23. Electrical stimulation of a r e a s 3a and 3b of the anterior part of the coronal gyrus also efficiently m o d u l a t e s the monosynaptic jaw closing and the disynaptic jaw o p e n i n g reflex t6"~7. However, stimulation of the perioral projection areas, 5a (anterior suprasylvian gyrus), 6aft (presylvian gyrus) and 43 (orbital gyrus), p r o d u c e s smaller effects mainly consisting of inhibition. These observations suggest that the axons of neurons located in the anterior part of the coronal and lateral sigmoid gyri project to the brainstem. In a m o r p h o l o g i c a l study, Yasui et al. ~4 confirmed that neurons located in the anterior part of the coronal and lateral sigmoid gyri p r o j e c t e d to the region of the trigeminal m o t o r nucleus and d e m o n s t r a t e d that fibers also projected directly to the brainstem from the lateral wall of the presylvian sulcus. This suggests that the lateral wall of the presylvian sulcus may function as the jaw and orofacial m o t o r cortex. Therefore, 3 separate jaw and orofacial m o t o r zones have been d e m o n s t r a t e d in the frontal cortex of cats: the coronal and lateral sigmoid gyri, the lateral wall of the suprasylvian sulcus, and the anterior part of the orbital gyrus. Landgren and Olsson '> studied the cortical p r o j e c t i o n of trigeminal afferents and showed that low-threshold trigeminal afferents p r o j e c t e d
to overlapping somatotopically organized fields in a r e a s 3a and 3b of the anterior coronal gyrus, to a r e a 6aft of the presylvian and anterior coronal gyrus, and to area 5a of the anterior suprasylvian gyrus. M o r e recently, Taira 2°'2~ r e p o r t e d a s o m a t o t o p i c r e p r e s e n t a t i o n of the intraoral structures in the anterior part of the coronal gyrus. These results suggest that the anterior part of the coronal and lateral sigmoid gyri and the lateral wall of the presylvian sulcus are related to the m o t o r function of the jaw and orofacial regions which is controlled by the non-noxious cutaneous sensory information from jaw and orofacial regions, The present study e x a m i n e d the cortical s e n s o r i m o t o r integration of jaw and orofacial regions in which both sensory input and ICMS were investigated at the same loci. A d d i t i o n a l l y , this study described spatial organization of i n p u t - o u t p u t coupling in the orofacial m o t o r zone of the anterior part of the coronal, the lateral sigmoid gyri and the lateral wall of the presylvian sulcus. E x p e r i m e n t s were p e r f o r m e d on 13 adult cats (2.5-3.5 kg) anesthetized with k e t a m i n e HC1 (initial dose of about 50 mg/kg, i.m.). The skull was o p e n e d over the coronal and lateral sigmoid gyri and a d j a c e n t regions, and the left eye ball was removed. A n acrylic c h a m b e r was placed over the skull opening and filled with mineral oil. The head was rigidly secured to a frame by means of s t a i n l e s s steel screws attached to the skull and e m b e d d e d in dental acrylic cement. Each animal was m a i n t a i n e d in a sedated
Correspondence: K. Iwata. Department of Physiology, School of Dentislry, Nikon University, 1-8-13 Kandasurugadai, Chiyoda-ku, Tokyo 101, Japan. 0006-8993/90/$(13.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)
338 state throughout the experiment by continuous intramuscular infusion of ketamine HC1 (10 mg/kg/1 h). Sedative level was judged by miosis and animal's movement. When the animal's pupil quickly responded to light presentation or animals made gross non-reflexive movement, additional ketamine HCI (10 mg/kg) was injected i.m. The traumatized tissues were infiltrated with 2% lidocaine-HC1 solution in order to prevent postsurgical pain during the experiment. Tungsten-in-glass microelectrodes were inserted into the coronal and lateral sigmoid gyri and the lateral wall of the presylvian sulcus to record unitary activities as well as to deliver ICMS. The electrodes were advanced through the cortex in 200 ltm steps. At each step, ICMS (0.2 ms, 12 cathodal pulses;
