Input-output relationships in the jaw and orofacial motor zones of the cat cerebral cortex

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; <30/~A, 300 Hz) was delivered. When movements were elicited, the threshold strength was measured, and repetitive stimulation (0.2 ms duration of cathodal pulses, 300 Hz) was applied at each site. The peripheral receptive fields of neurons surrounding the electrodes were examined by using natural stimulation (e.g. light touch to the facial skin, intraoral mucosa or the tooth). Jaw and orofacial movements were examined by visually inspecting muscle contraction and/or recording EMG responses from electrodes inserted into the jaw and orofacial muscles. The cortical sites were marked by passing a direct current (10 /~A, 10 s) through the electrodes and then histologically verifying their position after termination of the experiments. In 50 out of 71 penetrations of C-S motor zone, jaw and orofacial movements were produced by ICMS. Neurons were encountered along 43 tracks which could be driven by tactile stimulation of the facial skin, intraoral mucosa or tooth tap. In contrast, in 71 penetrations of the P motor zone, jaw and orofacial movements were produced by ICMS in only 19; cortical neurons in this zone received no cutaneous inputs from the orofacial regions. Penetrations from one cat are illustrated in Fig. 1A and B. Electrodes were inserted into the C-S motor zone and also into the P motor zone through the C-S motor zone. ICMS of an electrode inserted into the dorsal part of the coronal gyrus (track 9) produced eyelid lowering at a threshold intensity of 7/~A. A neuron located at the most effective position for ICMS-evoked eyelid movement also responded to tactile stimulation of the facial skin of the ear and eyelid regions. Stimulation of the border zone between the coronal and lateral sigmoid gyri (track 6) evoked jaw opening (stimulus threshold of 10 #A) and movement of the vibrissae at a stimulus threshold of 20 IrA. A neuron located at the most effective point along this track for evoking movements of jaw and vibrissae by ICMS responded to tactile stimulation of the contralateral lower molars. Neurons located in

the jaw movement zone frequently received periodontal inputs. In track 2, movement of the vibrissae was evoked by ICMS and the receptive field was restricted to the contralateral vibrissae and mandibular skin. In track 12, tongue movements were produced by ICMS (stimulus threshold of 4 /~A), and a neuron was found which responded to tactile stimulation of the contralateral tongue surface. At greater penetration depths, the electrode tips entered in P motor zone and complex patterns of movement were produced by ICMS: no neurons responded to tactile stimulation of the orofacial skin, mucosa or teeth. In track 12, repetitive stimulation of the most effective point evoked rhythmic jaw movements (stimulus threshold of 18/~A). Fig. IC,D,E and F illustrate two representative electrode tracks from one cat. The ICMS effect is shown at the right side of each track, whereas sensory inputs are noted at the left side. Electrodes were inserted into C-S and P motor zones and eyelid lowering was produced by ICMS in C-S motor zone (in tracks 3 and 4). Neurons located at the most effective point for evoking eyelid lowering by ICMS responded to tactile stimulation of the eyelid skin. A sample record of EMG and neuronal activity is shown in Fig. IE. In the P motor zone movements of the vibrissae, lower lip, and the tongue were simultaneously produced by the ICMS. Repetitive stimulation of the P motor zone produced rhythmic jaw movements in tracks 3 and 4. According to cytoarchitectonic criteria s, the most effective ICMS points along each track were located in lamina V of areas 3a, 6aft or 4y in the C-S motor zone or only in lamina V of area 6aft of the P motor zone (Fig. 1D). The results demonstrate that spatially specific inputoutput coupling exists throughout the jaw and orofacial motor zone of the C-S motor zone, whereas cortical cells in the P motor zone were related mainly to the output system serving the jaw and orofacial muscles. Jaw and orofacial movements in response to electrical stimulation of the cat cerebral cortex were first described by Ferrier 3 but have subsequently been described many times. Magoun et al. 1{)and Ward and Clark 22 obtained rhythmic jaw movement and lapping from electrical stimulation of the rostral part of the orbital and presylvian gyri. GaroP showed that stimulation of the rostral part of the coronal gyrus evoked tongue, lip. jaw and face movements. In a map of the cat's motor cortex, Woolsey23 located the jaw and orofacial motor zone in the rostral part of the coronal and presylvian gyri. The rostral part of the coronal gyrus described in these earlier reports corresponded to our C-S motor zone. According to the cytoarchitectonic criteria ~, the C-S motor zone was restricted to areas 3a, 6aft and occasionally to area 4y. Peripheral input to areas 3a and 3b of the coronal

339

E

C

A

EMG

......

Neuronal Activity PRSYL

ORB

]

" Smplkes

Brushing •.

.........

1o,

z,,. . . . . . . . .

~

l-o.v los

F

D

B

T9

T6

T2

T3

o

,o

.~ 37 e

T12 :v

ME

I

C-S M o t o r Zone

.:........ " ":.

T4 T3

RF

T4 JO ~

RjM

,e

?

P M o t o r Zone= RF

(-)

(-)

(-)

j

/~.~

~o 2,0 ~p.A

,)IPRSYL

(-1 Iv

v

m

Fig. 1. Penetration tracks accumulated from one cat are illustrated in A and B. A: photograph of the cortical surface illustrating sites of electrode penetrations. Each number indicates the penetrations. B: this shows the effects obtained from stimulation at different depths (rows) for each electrode track (columns). Each diagram shows the movement evoked by electrical stimulation of C-S and P motor zones at the lowest stimulus intensities along each track (solid region) and receptive fields of neurons located at the most effective site for evoking movements of the jaw and orofacial regions (shaded region). Numbers on each diagram show the stimulus threshold ~ A ) for each movement. Reconstruction of input-output coupling along tracks 3 and 4 in the C-S and P motor zones are illustrated in C,D,E and F. C: penetration tracks. D: tracing of frontal sections through the C-S motor zone and P motor zone. Electrodes were inserted into areas 3a, 6aft and 4V. Dotted line represents the lamina V. E: sample records of EMG activity from an eyelid muscle and of neuronal activity generated by tactile stimulation of the eyelid skin in track 3. The receptive field of this neuron is indicated by the arrow in F. F: motor effects on jaw and orofacial regions (right side) and receptive fields of neurons in C-S motor zone and P motor zone (left side) are represented on each track. ME, motor effects produced by ICMS; RF, receptive fields of neurons located in the most effective site; RJM, rhythmic jaw movement; PDL, periodontal membrane; JO, jaw opening; e, eyelid lowering; cv, movement of the contralateral vibrissae; iv, movement of the ipsilateral vibrissae; cp, movement of the contralateral perioral region; ip, movement of the ipsilateral perioral region; j, jaw movement; t, tongue movement; PRSYL, presylvian sulcus; COR, coronal sulcus; ORB, orbital sulcus.

gyrus and to a r e a 6aft of the p r e s y l v i a n and the lateral

the C-S m o t o r z o n e for jaw and o r o f a c i a l muscles, as

part

d e s c r i b e d p r e v i o u s l y in t h e h a n d m o t o r z o n e l"2~2"'-~~s'jg.

of the

anterior

sigmoid

gyri was

described

by

L a n d g r e n and O l s s o n 9. S y s t e m i c analysis of the cortical

A g g r e g a t e s of cells in the C-S m o t o r z o n e h a v e c u t a n e o u s

field p o t e n t i a l s s h o w e d that t h e s e gyri i n c l u d e d s o m a t o -

p e r i p h e r a l r e c e p t i v e fields r e l a t e d to the skin a r o u n d the

topically o r g a n i z e d , but o v e r l a p p i n g , oral and p e r i o r a l

m o v i n g r e g i o n (Fig. 1 B , E and F), as also d e s c r i b e d in the

s o m a t o s e n s o r y p r o j e c t i o n fields. T h e s e results t a k e n t o g e t h e r with t h o s e of O l s s o n and L a n d g r e n 16, and

hand motor zone.

O l s s o n et al.'7 suggest that the rostral part of the c o r o n a l , the lateral part of the a n t e r i o r sigmoid and the p r e s y l v i a n

was l o c a t e d in the d e e p r e g i o n of the lateral wall of the p r e s y l v i a n sulcus. P r e v i o u s a u t h o r s 3"4"6"~''°1~22"23 w e r e

gyri h a v e i n p u t - o u t p u t f u n c t i o n s in the jaw and orofacial

u n a b l e to a c t i v a t e p y r a m i d a l cells of this r e g i o n using

m o t o r z o n e . In the p r e s e n t study, direct e v i d e n c e was

surface e l e c t r o d e s and c o n s e q u e n t l y did not d e s c r i b e this m o t o r z o n e . A n a t o m i c a l tracing t e c h n i q u e s h a v e s h o w n

o b t a i n e d for tight c o u p l i n g of i n p u t - o u t p u t r e l a t i o n s in

In c o n t r a s t to the C-S m o t o r z o n e , the P m o t o r z o n e

34O that in the lateral wall of the presylvian sulcus there are

observed during repetitive st i m u l am m ot the P motor

many lamina V cells, which project to the adjacent

zone. In many earlier reports -~'4~ "-~" J~]~:~, repetitive

regions of the trigeminal m o t o r nucleus ca. T h e r e f o r e ,

stimulation to the rostral part of the orbital gyrus evoked

cortical neurons in P m o t o r zone have projection fibers

rhythmic jaw and tongue m o v e m e n t s . This area was

descending to the trigeminal m o t o n e u r o n s via the pyra-

described as a cortical masticatory area. The P mot or

midal tract. F u r t h e r m o r e , ICMS of the P m o t o r zone

zone described

produced

masticatory area. T h e r e f o r e , two masticatory areas exist

co-ordinated

bilateral m o v e m e n t s ,

whereas

in this study

is separated

from the

I C M S delivered to the C-S m o t o r zone produced simple

in the cat m o t o r cortex. A n a t o m i c a l study described that

muscle twitches on the contralateral side of the jaw and

cortical cells located in the P m o t o r zone had a denser

orofacial regions.

projection to the adjacent region of trigeminal m o t o r

These data support the hypothesis that sensory inputs

nucleus than did the orbital cortex 24. This suggests that

of the orofacial regions may assist jaw and orofacial

the descending fibers from the P m o t o r zone may control

m o v e m e n t s in the C-S m o t o r zone, thereby suggesting a

the brainstem masticatory rhythm generator, whereas

m o d u l a t o r y role for the cortex in the production of jaw

those in the orbital cortex may control the masticatory

and orofacial m o v e m e n t s . On the other hand, the P

m o v e m e n t via an o t h er cortical area.

m o t o r zone has only a c o m m a n d function in the control of rhythmic jaw, tongue m o v e m e n t s and orofacial move-

of facial muscles. Rhythmic jaw m o v e m e n t s were also

We are grateful to Dr. K. Kanda for comments on the manuscript, and to Drs. E.H. Chudler, D.R. Kenshalo Jr., R.L. Nahin and J.D. Stephenson for revising the English. This study was supported in part by a Grant-in-Aid for Scientific Research (60480403) from the Japanese Ministry of Education, Science and Culture.

1 Asanuma, H. and Sakata, H., Functional organization of a cortical efferent system examined with focal depth stimulation in cats, J. Neurophysiol., 30 (1967) 35-54. 2 Asanuma, H., Stony, S.D. and Abzug, C., Relationship between afferent input and motor outflow in the cat motor sensory cortex, J. Neurophysiol., 31 (1968) 679-681. 3 Ferrier, D., The Functions of the Brain, 2nd edn., Smith Elder, London, 1886. 4 Garol, H.W., The 'motor' cortices of the cat, J. Neuropathol. Exp. Neurol., 1 (1942) 139-145. 5 Hassler, R. and Muhs-Clement, K., Architectonischer Aufbau des sensomotorischen und parietalen Cortex der Katze, J. Hirnforsch., 6 (1964) 377-420. 6 Hess, W.R., Akert, K. and MacDonald, D.A., Functions of the orbital gyrus of cat, Brain, 75 (1952) 244-258. 7 Iwata, K., Itoga, H., Hanashima, N. and Sumino, R., Movements of the jaw and orofacial regions evoked by stimulation of two different cortical areas in cats, Brain Research, 359 (1985) 332-337. 8 Kawamura, Y. and Tsukamoto, S., Analysis of jaw movements from the cortical jaw motor area and amygdala, Jap. J. Physiol., 10 (1960) 471-488. 9 Landgren, S. and Olsson, K.A., Low threshold afferent projections from the oral cavity and face to the cerebral cortex of the cat, Exp. Brain Res., 39 (1980) 133-147. 10 Magoun, H., Ranson, S.W. and Fisher, C., Corticofugal pathways for mastication, lapping and other motor functions in the cat, Arch. Neurol. Psychiatry, 30 (1933) 292-308. 11 Morimoto, T. and Kawamura, Y., Properties of tongue and jaw movements elicited by stimulation of the orbital gyrus in the cat, Arch. Oral Biol., 18 (1973) 361-372. 12 Murphy, J.T., Wong, Y.C. and Kwan, H.C., Afferent-efferent linkages in motor cortex for single forelimb muscle, J. Neurophysiol., 38 (1975) 990-1014. 13 Murphy, J.T., Kwan, H,C., MacKay, W.A. and Wong, Y.C., Spatial organization of precentral cortex in awake primates. III. Input-output coupling, J. Neurophysiol., 41 (1978) 1132-1139.

14 Nakamura, Y. and Kubo, Y., Masticatory rhythm in intracellutar potential of trigeminal motoneurons induced by stimulation of orbital cortex and amygdala in cats, Brain Research, 148 (1978) 504-509. 15 Nieoullon, A. and RispaI-Padel, L., Somatotopic localization in cat motor cortex, Brain Research, 105 (1976) 405-422. 16 Olsson, K.A. and Landgren, S., Facilitation and inhibition of jaw reflexes evoked by electrical stimulation of the cat's cerebral cortex, Exp. Brain Res., 39 (1980) 149-164. 17 Olsson, K.A., Landgren, S. and Woodberg, K.G., Localization of, and principal convergence on, the inter neuron in the disynaptic path from the coronal gyrus of the cerebral cortex to the trigeminal motoneurons in the cat, Exp. Brain Res., 65 (1986) 83-97. 18 Rosen, I. and Asanuma, H., Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-output relations, Exp. Brain Res., 14 (1972) 257-273. 19 Sakata, H. and Miyamoto, J., Topographic relationship between the receptive fields of neurons in the motor cortex and the movements elicited by focal stimulation in freely moving cats, Jap. J. Physiol., 18 (1968) 489-507. 20 Taira, K., The representation of the oral structures in the first somatosensory cortex of the cat, Brain Research, 409 (1987) 41-51. 21 Taira, K , Characteristics of periodontal mechanosensitive neurons in the first somatosensory cortex of the cat, Brain Research, 409 (1987) 52-61. 22 Ward, J.W. and Clark, S.L., Specific responses elicited from subdivision of the motor cortex of the cerebrum of the cat, J. Comp. Neurol., 63 (1935) 49-64. 23 Woolsey, C.N., Organization of somatic sensory and motor areas of the cerebral cortex, In H.F. Harlow and C.N. Woolsey (Eds.), Biological and Biochemical Bases of Behavior, Vol. 6l, University of Wisconsin Press, 1969, pp. 73-166. 24 Yasui, Y., Itoh, K., Mitani, A. and Takada, M., Cerebral cortical projection to the reticular regions around the trigeminal motor nucleus in the eat, J. Comp. Neurol., 241 (1985) 348-356.

ments without the support of peripheral inputs. In the present study, ICMS to P m o t o r zone produced not only jaw and tongue m o v e m e n t s but also m o v e m e n t s