Jpn. J. Oral Biol., 33: 592-599, 1991.

ORIGINAL

Jaw and orofacial motor representation

in cat orbital

Yoshiyuki Tsuboi, Koichi Iwata, Hiroyuki Muramatsu,

Junichi Yagi, Yuji Inomata, Reo Kikuta,

Keiji Yoshii and Rhyuji Sumino

Department of Physiology, Nihon University. School of Dentistry, 1-8-13 Kandasurugadai, Chiyoda-ku, Tokyo 101, Japan (Director: Prof. Rhyuji Sumino) Accepted for publication: June•k 20, 1991•l

Key words: motor effect/trigeminal nerve/orbital gyrus/ICMS/cat

Abstract: Jaw and orofacial motor representation in the orbital cortex was studied by intracortical

microstimulation (ICMS) in lightly anesthetized cats. ICMS of the posterior portion of the the orbital

gyrus produced movements of facial muscles, whereas stimulation of the anterior portion of the orbital

gyrus produced more generalized movement of facial, jaw and tongue muscles. The region producing jaw movements was more restricted than the regions producing tongue and facial movements. Repe- titive stimulation of the anterior orbital gyrus produced either rhythmic jaw movements or sustained

jaw opening. Cytoarchitectonically, the posterior portion of the orbital gyrus was restricted to area 43 and the anterior portion to areas 43 and 6 aƒÀ.

present study, the function of the orbital gyrus Introduction was studied by detailed topographic mapping The orbital cortex in the cat has been ter- of the effects produced by ICMS and the med the cortical masticatory area because results correlated with the cytoarchitectonic criteria of Hassler and Muhs-Clement7). repetitive stimulation of its anterior part pro- duces rhythmic jaw and tongue move- Materials and Methods ments1-3). The axons of cells in this cortical region may project to a "pattern generator" Experiments were performed on 16 cats in the rhythmic generation of masticatory anesthetized initially with Ketamine HCL (50 jaw movements2,4). However, it was shown mg/kg i. m.). During surgery, anesthesia that intracortical microstimulation (ICMS) of was maintained with a mixture of halothane, the same area produced not only movements nitrous oxide, and oxygen and anesthetic level of the jaw and tongue but also of the facial was maintained throughout the experiment muscles suggesting that the orbital cortex of by intramuscular infusion of Ketamine HCl the cat was involved in both orofacial and (20 mg/kg/h). Additionally, incision sites masticatory motor function5). Earlier stud- were infiltrated with a 2% lidocaine HCl es1-3,6) did not determine the most effectivei solution. Heart rate was continually mon- sites which evoked jaw and orofacial move- itored by recordings of EKG. Gas anesthesia. ments because the stimulation electrodes were was discontinued after the surgery. Anes- placed on the surface of the cortex. In the thetic level was judged by miosis, animal's Y. Tsuboi et al.: Jaw and orofacial motor representation in cat orbital gyrus 593

movement and heart rate. When animal's appropriate. EMG activities of each muscle

pupil quickly responded to light presentation and minimum latencies to contraction were or animal made gross non-reflexive move- determined by using suprathreshold current to ment or the heart beat rate was changed evoke an EMG response. When jaw and during electrical stimulation of the cortex , tongue muscle contractions were elicited, re- additional ketamine HC1 (20 mg/kg) was in- petitive stimulation at a frequency of 30 Hz jected i. m. Body temperature was continu- (stimulus current less than 30 ƒÊA, 0.2 ms pulse ously monitored with a rectal probe and main- width) was applied to see if it produced sus-

tained between 37•Ž and 39•Ž with a heat- tained jaw opening or rhythmic jaw move-

inguAd. The animal's head was fixed rigidly ment. Jaw and orofacial muscle contractions to a head-holder by means of skull screws were analyzed and lesions were placed in

and dental acrylic cement. The left eyeball selected penetrations at the end of each ex- and the marginal region of the maxillary periment byuAssing direct current (10 ƒÊA, 10 s) bone were removed to give access for the through the electrodes to facilitate histolo- electrodes to the orbital cortex. The skull gical examination. over the coronal and was re-

moved and an acrylic resin chamber was insta- Results lled over the opening. The cisterna magna

was then opened to allow cerebrospinal fluid 1. Cortical representation of the jaw and to drain away and to prevent swelling of the orofacial motor zones brain. The acrylic chamber was filled with Fig. 1 shows sample penetration tracks from mineral oil after removing the dura from the one cat in which movements of jaw, tongue orbital and coronal gyri. Electrode penetra- and face were produced by ICMS of less than tions were placed 0.5 mm or less auArt in the 30 ƒÊA (Eyelid lowering was analyzed only orbital cortex and were made into the orbital on the contralateral side because the left eye- gyrus and cortical area extending to the pre- ball had been removed for installation of the sylvian . Each penetration was made acrylic chamber). ICMS delivered to the an- as near perpendicular to the cortical surface terioruArt of the orbital gyrus evoked eyelid as possible and was observed through a mi- lowering, movements of vibrissae, lower lip, croscope and photographed. jaw and tongue, whereas only eyelid lowering Each grass-coated tungsten microelectrode was observed after ICMS of the posterior (10-20 pm of tip diameter) was advanced rt (Fig. 1 B and C). Thus the uA anterior through the cortex in 200 pm steps and ICMS portion of the orbital gyrus was termed the "jaw (twelve 0.2 ms cathodal pulses,<30 ƒÊA, 300 , tongue and facial motor zone" (Fig. 1 Hz with 40 ms train duration) applied after Ca) and the posterior portion, the "facial

each step, according to Asanuma's tech- motor zone" (Fig. 1 Cb). Stimulation of

niques8,9). We accumulated the effective points the posterior portion of the orbital gyrus (tracks

activated by ICMS of less than 30 ƒÊA, on 9 and 10) produced eyelid lowering. In

the basis of Sessle and Wiesendanger's cri- addition to eyelid lowering, movements of the

teria16). They have shown that ICMS of less vibrissae and lower lip were evoked from

than 30 ƒÊA upper limit defines an excitable tracks 7 and 8. Movement of facial muscles

region of the limb , which con- and jaw opening were produced from stimula-

tains nearly all physiologically as well as ana- tion in track 6 and of the vibrissae, lower

tomically identified cortico-spinal projection lip and tongue from stimulation in tracks 3

elements16). Once a muscle movement had and 4. Stimulation of the most anterioruArt

been identified by two independent observers, of the orbital gyrus (tracks 1 and 2) evoked

the fine muscle contractions were examined movements of the lower lip and tongue.

both visually and byuAluAtion. When Jaw movements were obtained from ICMS threshold intensities less than 10 ƒÊA were of an area just adjacent to the anterior end of observed, bipolar wire electrodes were placed orbital sulcus (tracks 5 and 6). These results acutely in jaw, tongue and facial muscles, as demonstrated that the jaw, tongue and oro- 594 Jpn. J. Oral Biol., 33: 592-599, 1991.

A B

C D

T4 T6 T10

Fig. 1 Tracks represented on the cortical surface from which movements of the jaw and orofacial muscles were evoked by ICMS in one cat. A=photograph of the cortical surface of the orbital gyrus and adjacent region of the cat frontal cortex. B=table indicating the penetration tracks and threshold intensities for evoking movements on jaw and orofacial regions. Penetration tracks are numbered from 1 to 10 along the abscissa. The numbers in each frame indicate the stimulus threshold (in ) for producing each movement. eye l.=eyelid lowering, vibrissae=movement of vibrissae,uA lower lip=movement of lower lip, j. o.=jaw opening, j. c.=jaw closing, tongue=tongue move- ment. C=schematic drawing of the orbital gyrus. The two regions of the orbital gyrus (a, b) are seuArated by a dotted line; the line between a and b is vertical to the orbital sulcus. D= sample records of EMG activites of jaw and orofacial muscles at tracks 4, 6 and 10. Note that tracks 1 to 8 are located in the anterior portion of the orbitalgyrus (a) and tracks 9 and 10 are in the posterior portion (b). COR=coronal sulcus, ORB=orbital sulcus, PRESYL=presylvian sulcus, RHIN=, cl=contralateral lower lip, il=ipsilateral lower lip, cv=contralateral vibrissae, iv=ipsilateral vibrissae, e=eye lid lowering, t=tongue movement, c. dig=contralateral digastric muscle, i. dig=ipsilateral digastric muscle.

facial motor zones were represented on the obtained from 155 tracks were as follows: 33.5 orbital gyrus along the orbital sulcus. Further- 7.5 ms for facial muscles (Fig. 2 A); 31.5•} •} more, it can be seen that the largest repre- 8.1 ms for tongue muscle (Fig. 2 B); 25.5•} sentation within this effective region was 4.4 ms for masticatory muscles (Fig. 2 C). devoted to the facial musculature, as described These results indicate that latencies for EMG for the conscious monkey10). In the present activities of facial and tongue muscles were study, the orbital gyrus was seuArated into statistically longer than those of masticatory two different jaw, tongue and orofacial motor muscles (p<0.01: Mann-Whitney U test) zones (shown as a and b in Fig. 1 C). Sam- and that there were no differences between ple records of EMG activities evoked by sti- facial and tongue muscles. mulation of each of these zones are shown 2. Intracortical representation of the jaw in Fig. 1 D. The mean latencies (•}standard and orofacial motor zones deviation) of EMG activities following ICMS In the present study, a total of 571 loci Y. Tsuboi et al.: Jaw and orofacial motor representation in cat orbital gyrus 595

A B C

Fig. 2 Histogram of the distribution of the minimum latencies complied from EMG records of respo nses evoked by suprathreshold ICMS. Histograms of latencies of EMG activities recorded from A= facial muscles, B=tongue muscles, C masticatory muscles .

were effective in producing movements of the evoked, were located at depths between 1 .5 jaw and orofacial regions with ICMS of less and 2.5 mm from the cortical surface and the

than 30ƒÊA. Of these effective sites, 55% intracortical distribution of the effective points

were involved in facial muscles, 1% in mas- were similar for each movement. In contrast, ticatory muscles, 10% in tongue muscles, 27 only tongue movements were produced by

% in both facial and tongue muscles and 7% stimulation of the most anterior portion of

in facial, tongue and masticatory muscles . the gyrus (track 33). The most effective

Fig. 3 shows the intracortical distributions point was restricted to lamina V where

of the most effective points in each track. large pyramidal cells were found . Thus, this

Abscissa of each histogram indicates the intra- particular depth corresponded to lamina V of cortical distribution of effective points evok- area 6 aƒÀ.

ing movements at stimulus intensities of less

than 30ƒÊA. Eyelid lowering had the lowest Discussion threshold, less than 1ƒÊA. Cytoarchitectoni-

cally, the most effective points for each move- The present experiments demonstrated that

ment were restricted to laminae III and V ICMS in orbital gyrus and adjacent regions

of areas 6 aƒÀ and 43 (Fig. 3). Stimulation produced not only jaw and tongue move- with electrodes inserted into the anterior ments but also movements of facial muscles.

(tracks 21, 28, 33 and 25) portions of the orbital This region was subdivided into two regions , "the jaw gyrus evoked twitches of tongue and facial , tongue and facial motor zone"

muscles (Fig. 4). Simultaneous movements (Fig. 1 Ca) in the anterior portion of the in tracks 21 and 28; repetitive stimulation orbital gyrus and "the facial motor zone"

of the most effective points along these tracks (Fig. 1 Cb) in the posterior portion. Thus,

produced rhythmic jaw movements and sus- it is suggested that the orbital gyrus subserves

tained jaw opening, respectively. The most a motor function for jaw and tongue move- effective sites from which movements were ments and also for movements of the facial 596 Jpn. J. Oral Biol., 33: 592-599, 1991.

A stem rhythm generating center (pattern-gene- rator, see references 2, 3). In the present

study, repetitive ICMS to a very restricted

anterior part of the orbital gyrus (less than

1 mm2) produced either a complex pattern of

rhythmic jaw and tongue movements or sus

tained jaw opening. Previous studies1,2,6) did

not describe such a localized representation

probably because of different methods of sti- mulation (e. g. surface stimulation vs. ICMS).

Surface stimulation with large electrodes, would

tend to obscure the pattern of organization

observed in the present experiments, because

of wide (2-4 mm2) current spread12).

Cytoarchitectonic studies revealed that the

jaw, tongue and facial motor region was re- stricted to areas 6 aƒÀ and 43 whereas rhythmic

jaw and tongue movements were produced only by repetitive stimulation of area 6 aƒÀ.

The large pyramidal cells located in lamina

V of the motor cortex (areas 6 aƒÀ and 4ƒÁ)

project to the spinal cord7), presumably via the pyramidal tract. In the anterior portion

of the orbital gyrus, ICMS to one location

produced simultaneous movements of jaw, tongue and facial muscles (Fig. 4) and there Fig. 3 Relationship between number of the most was no clear somatotopic representation. Pat- effective points in each track and intrala- terns of movements produced by ICMS to minal distribution of the effective points. this area were more complex than those in A=histograms of distribution of the the fore- and hindlimb primary motor cor- intralaminal effective points in the ante- tex13-17). Morimoto et at.2) showed that two rior portion, B=those in the posterior different types of jaw and tongue movements portion. could be obtained from repetitive stimulation of the anterior part of the orbital gyrus and muscles. they suggested that there were two different

The anterior portion of the orbital gyrus pathways from orbital gyrus to the brain stem, has been considered as the cortical masticatory one for each type of jaw and tongue move- area in the cat, because repetitive surface ments. Olsson and Landgren18) described stimulation of this area produces rhythmic that electrical stimulation of area 6 aƒÀ of the jaw and tongue movements1-3,6.. A HRP anterior portion of the orbital, coronal and study4) revealed that cortical cells from this lateral sigmoid gyri affected the jaw opening region send their axons to the pontine reflex in response to electrical stimulation of bulbar reticular region via the pyramidal tract. the trigeminal nerve, while stimulation of Neurons in this area were antidromically area 43 of the middle portion of the orbital

activated by stimulation of the pyramidal gyrus did not consistently affect the reflex. tract or reticular regions around the trige- This suggests that there are two different

minal motor nucleus11). pathways from the anterior portion of the These reports suggest that cortical neurons orbital gyrus to the brain stem, an indirect

located in the anterior part of the orbital pathway in which cortical cells located in the gyrus control the jaw and tongue movements jaw, tongue and facial motor zone of area 43 by means of axons projecting to the brain in the anterior and posterior portions of the

B Y. Tsuboi et al.: Jaw and orofacial motor representation in cat orbital gyrus 597

A

B 598 Jpn. J. Oral Biol., 33: 592-599 , 1991.

orbital gyrus send axons to the brainstem portion, but not of area 43 of the middle via the anterior cortical area and a descend- portion of the orbital gyrus, produced clear ing pathway in which axons of the cortical effects on the jaw reflex. These results cells located in the jaw, tongue and facial suggest that cortical cells in the middle portion motor zone of area 6 aƒÀ in the anterior portion of the orbital gyrus have longer descending of the orbital gyrus project to the brain pathways than cells in the anterior portion stem. Furthermore, we found a wide range of the orbital gyrus and raise the possibility of latency distribution of EMG activities in that cortical cells located in the middle part

jaw and orofacial muscles which showed simi- of the orbital gyrus may send their axons to lar values as described by Huang et al .10). the brain stem via another cortical region. This result suggests strongly the existence of

multiple descending pathways from the orbital Conclusion cortex to the brainstem.

In previous studies1, 2, 6, 19) on the motor 1) ICMS of the posterior poition of the

effects of the orbital cortex, the motor area orbital gyrus produced movements of facial

was restricted to the jaw and tongue motor muscles, whereas stmulation of the anterior

zones and movements of the facial muscles portion of the orbital gyrus produced more

were not described. The present study found generalized movemnt of facial, jaw and ton-

the facial motor zone (movements of vibri- gue muscles. ssae, lower lip and eyelid lowering) to be 2) The region producing jaw movements

represented in the jaw and tongue motor zones . was more restricted than the regions produc- ICMS in the posterior part of orbital gyrus ing tongue and facial movements.

produced only eyelid lowering. Regions 3) Repetitive stimulation of the anterio-

producing movements of the vibrissae and orbital gyrus produced either rhythmie jaw lower lip overlapped and were represented opening.

predominantly in the middle and anterior 4) Cytoarchitectonically, the posterior por-

portions of the orbital gyrus. Hence. each tion of the orbital gyrus was restricted to facial motor portion did not have a so- area 43 and the anterior portion to areas 43

matotopic representation as described for the and 6 aƒÀ.

cat 8, 9, 13-15). Cytoarchi-

tectonically. facial motor zones were restric- Acknowledgments

ted to area 43 in the posterior and middle We thank Dr. B. J. Sessle and Dr. K. Kanda portions of the orbital gyrus and areas 6 aƒÀ for helpful comments on this manuscript, and to and 43 in the middle and anterior portions; Drs. J. D. Stephenson, E. H. Chudler and D. there are no large pyramidal cells in area 43 R. Kenshalo, Jr. for revising the English. in the posterior and middle portions of the orbital gyrus but many large pyramidal cells in area 6 aƒÀ in the anterior portion 7). More- over, the latency of EMG activities of facial muscles were much longer than those of the masticatory muscles. Furthermore, Olsson and Landgren 18) reported that the electrical stimulation of the area 6 aƒÀ of the anterior

Fig. 4 Reconstruction of a track in exp . C-46 from which movement of both sides of the lower lips , the vibrissae, tongue and jaw were evoked by ICMS of the anterior (T 21, T 28 and T 33) and middle( T25) portions of the orbital gyrus. A=penetration points and sectional orientation plotted on the cortical surface and penetrations shown for each plane . Small dots represent the laminaV cells . B=threshold-depth relation plot for the microelectrode track . Abbreviations indicate movement of cl=the contralateral side of the lower lip , il=the ipsilateral side of the lowerlip, cv=the ipsilateral side of the vibrissae,iv=the ipsilateral side of the vibrissae , t=tongue. Y. Tsuboi et al.: Jaw and orofacial motor representation in cat o rbital gyrus 599

抄 録:皮 質 内 微 小 刺 激 法(ICMS)を 用 い ,軽 度麻 酔 ネ コ の大 脳 皮 質 眼 窩回 にお け る顎,顔 面 口腔領 域 の 運 動 野 の配 列 を検 索 した 。 眼 窩 回 後 方 部 のICMSは ,顔 面 筋 の 収縮 を引 き起 こ し,眼 窩 回 中 央 部 のICMS は,顔 面 お よび 顎 筋 両 者 の収 縮 を引 き起 こ した 。眼 窩 回 前方 部 のICMSで は,顔 面 ,顎 お よ び 舌 の動 きが 生 じた。 顎 運 動 を生 じ る皮 質領 域 は ,舌 お よび 顔 面 の 動 きを生 じる領 域 よ り狭い範 囲 で あ った 。眼 窩 回 前 方 部 の頻 回 刺 激 で は,リ ズ ミカ ル な 顎運 動 ま た は ,持 続 的 開 口運動 が誘 発 され た 。 細 胞 構 築 学 的 に は,眼 窩 回後 方 部 は43野 で,前 方 部 は,43野 と6aβ 野 に ま たが って い た 。

References and electrophysiological identification of affe- rent input and corticobulbar projections. J. 1) Magoun, H. W., Ranson , S. W., and Fis- Neurophysiol. 59: 796-818, 1988. her, C.: Corticofugal pathways for masti- 11) Lund, J. P. and Sessle, B. J .: Oro-facial cation, lapping and other motor functions in and jaw muscle afferent projections to neur- the cat. Arch. Neurol. Psychiat . 30: 292- ons in cat frontal cortex. Exp. Neurol. 45: 308, 1933. 314-331, 1974. 2) Morimoto, T. and Kawamura, Y .: Proper- 12) Woolsey, C. N.: Organization of Somatic ties of tongue and jaw movements elicited by Sensory and Motor Areas of the Cerebral stimulation of the orbital gyrus in the cat. Cortex. (Harow, H. F. and Woolsey, C. N., Arch. Oral Biol. 18: 361-372, 1978. eds.: Biological and Biochemical Basis of 3) Nakamura, Y. and Kubo, Y.: Masticatory Behaviour). pp.73-166, University of Wis- rhythm in intracellular potential of trige- consin Press, 1969. minal motoneurons induced by stimulation 13) Nieoullon, A. and Rispal-Padel , L.: Soma- of orbital cortex and in cats . totopic localization in cat motor cortex. Brain Res. 148: 504-509, 1978. Brain Res. 149: 405-422, 1976. 4) Yasui, Y., Ito, K., Mitani, A., Takada, M. 14) Pappas, C. L. and Strick, P. L.: Physiolo- and Mizuno, N.: Cerebral cortical projec- gical demonstration of multiple representation tion to the reticular regions around the tri- in the forelimb region of the cat motor geminal motor nucleus in the cat. J. Comp. cortex. J. Comp. Neurol. 200: 481-490, Neurol. 241: 348-356, 1985. 1981. 5) Iwata, K., Itoga, H., Hanashima , N. and 15) Pappas, C. L. and Strick, P. L.: Anato- Sumino, R.: Movements of the jaw and mical demonstration of multiple representa- orofacial regions evoked by stimulation of tion in forelimb region of the cat motor two different cortical areas in cats. Brain cortex. J. Comp. Neurol. 200: 491-500, 1981. Res. 359: 332-337, 1985. 16) Sessle, B. J. and Wiesendanger, M.: Stru- 6) Hess, W. R., Akert, K. and McDonald, D. ctural and functional definition of the motor A.: Functions of the orbital gyrus of cat. cortex in the monkey (macaca fascicularis) . Brain 75: 244-258, 1952. J. Physiol. 323: 245-265, 1982. 7) Hassler, R. and Muhs-Clement, K.: Archi- 17) Iwata, K., Muramatsu, H., Tsuboi, Y. and tectonishe aufbau des Sensomotorishen und Sumino, R.: Input-output relationships in Parietal Cortex der Katze. J. Hirnforsh 6: the jaw and orofacial motor zones of the 377-420, 1953. cats . Brain Res. 507: 337- 8) Asanuma, H. and Sakata, H.: Organization 340, 1990. of a cortical efferent system examined with 18) Olsson, K. A. and Landgren, S.: Facilli- focal depth stimulation in cats. J. Neurophy- tation and inhibition of jaw reflexes evo- siol. 30: 35-54, 1967. ked by electrical stimulation of the cat's 9) Asanuma, H., Stony, S. D. Jr. and Abzug, cerebral cortex. Exp. Brain Res. 39: 149-164, C.: Relationship between afferent input and 1980. motor cortex in the cat. Brain Res. 172: 19) Sumino, R., Tamura, K., Itoga, H., Iku- 197-208, 1968. kawa, A. and Iwata, K.: Input-output re- 10) Huang, C. S., Sirisko, M. A., Hiraba H., lations between two separate orofacial motor Murray, G. M. and Sessle, B. J.: Organi- areas of the cat cerebral cortex. Pro. Int. zation of the primate face motor cortex as Union Physiol. Soc. 16: 193, 1986. revealed by intracortical microstimulation