THE REPRESENTL4TION OF FACIAL AND SCAIJP MUSCLES I N THE FACIAL STCLEUS

JOHN SZENTAGOTHAI Uepurtiuent of d ~ t n t o ? i i y , Universi fy of PPcs, Hiinqary

FIVE FIGURES

ISTRODUCTION

In most of the riiotor nuclei the ganglion cells are not uni- fomily distributed throughout the whole nucleus. They are grouped into several iiiore or less distinct cluinps, some of which possess cells which differ in size and appearance from the others. These cell clumps are very generally believed to possess a definite relation to the several branches of the nerve and tlie muscles they supply. Reviewing the literature dealiiig with this subject, we notice that the opinions of most authors concerning representation of the different muscles in tlie cell clusters of their nuclei are very contradictory. I n investiga- tions on this subject the chroniatolytic nietliod was generally used. Even working on tlie same animal and with the same nietliods authors got different results, as can be seen in cake of the ocnlomotor nucleus, where the nuclear representation, a question of great practical value, was often investigated. C’oncerning other cranial motor nuclei the situation is very siniil a r.

Several years ago we (Szenthgothai, ’41) introduced a new tecliiiique in order to deterniine the exact representation of iiinsclcs in their supplying nuclei which we believe to be much more suitable for this purpose than the clironiatolytic method. K i t h the aid of a stereotasic instrument, very similar to the well-known Horslep-Clarke apparatus, we mere able to prove

’707

208 JO H N S Z E X T k O T HA1

by aiintoniic aiicl plipsiologic evicleiice, that tlie representation of eye muscles in the ocnloriiotor iiiwletis is just tlie reverse of tlie well liiiowii description of Beriilieiiiier ( 1X9i ) , the in- ferior rectus heiiig localized in the frontal and the huperior ~ e c t u s in the caudal p a r t of the nucleus. Later, we deteriiiiiied tlie i.epresentation of tlie laryngeal muscles iii the nucleus aiiiliiguus (Szcnthgothai, ’43).

C’onceriiiiig the iiuclear representation of the facial aiid scalp iiiuscles there a re d i f fc iwt and partly coiiti.aclictorJ- theoi*ies hasetl oil the clironiatolytic iiichthocl, wliich we caiiiiot beliere to give exact results. K e therefore attempted to find out with tlie aid of our new method tlie real representation of t’acinl iiiuscles in this nucleus.

TECHNIQrE

Our experiiiients were iiiatle 011 adult cats with the aid of a stei.eotaxic ins trnrnen t, modified a f te r tlie well-knomi prin- ciple of Horslq- niicl C’larlie (’0s). \T’e used bipolar iiecdles of 0.25 iiiiti cliaineter (platiiiuiii wire of 0.1 111111 aiitl glass in- su la t ion ) for f a r it clic stimulation. S t iriiula t io ii esp e rim en t 4

provide only preliiiiinary orientation iii such cases, hut they arc w r p useful. I n a series of 20 successful experiments small electrolytic lesions (3 J2A aiioclal, uiiipolar electrode of 0.13 iiiiii. cliaiii.) of about 0.5 iiiiii in dimicter were placed in dif- ferent parts of’ the nucleus (fig. 1 aid 2) . We sncceccl(d in plaeiiig sevei-a1 lcbsioiis in tlie mcclial, lilteral, anterior, poste- rior, superior aiicl inferior par t s of the nucleus. Soiiie lesions were placed tangentially iicar the iricclinl o r lateral sitle, oral aiid Ci11ldaI ~11~1s of t h o ~ i ~ c l e ~ s in order to deqtroy olilp :I

siiiall 11111iiher of gmiglioii cells 011 its border. Special care was takcri riot to sever the eiiiergiiig roots of tlie nerve. Tlie iieetlle was insclrtcd into the brain froin tlie occiput. I n 2 cabe< tlie lesions were plactd dorsal am1 dorsolatcral to the i iuc l~us in order t o destroy tlie s c a t t e i d acres~oi’p cells also. Tlie facial iiiotilitJ- of the operated animals was carefnlly 4uilied a d recorded iii each case. Four or 5 clays af tcr o1)cratioii when ti-auniat ic degeneration of nerve fibers (asoiis) and

REF’IlESEN TATIOX O F FACIAL JIVSCLES 209

Fig. 1 A. Electrolytic lesion in the rentral par t of the f ac i a l iiacleur. E. Situ- ation of the photomicrograph on the cross section of the braiii stein. r.cl.V., radix descriideiis iien i trigeiiiiiii; iiu.T’II., facial iiiicleus.

Fig. 2 A. Electro1,vtic lesion in the rentrolnteral par t of the facial nucleus. B. Situation of the pliotoniierograph on the cross section of the b r a i n stem. r.d..V., radix desceiideiis nervi trigemini; iiii.VII., facial nucleus.

210

REPRESENTATION OF F.4CIAL MUSCLES 211

motor end-plates was manifest the cats were killed and frozen sections of the clifferelit branches of the facial nerve and of the niuscles were staiiiecl by the method of Rielschowsliy- Gross. In the nerve branches and muscles we tried to estimate approxiinate1;v the numbers of degenerated and normal fibers or end-plates.

OBSERVATIOXS

Stiinulatioii of the medial part of the facial nucleus geiier- ally resulted in contractions of the platysma and auricular muscles. KO contractions of the muscles around the eye or of the frontal region could be observed during stimulation of the medial part. Movements of the lips occurred when tlie an- terior part was stimulated. During stimulation of tlie lateral part of the iiucleus, orbicular and frontal contractions were most frequently apparent. Contractions of the supraliyoid muscles were obtained by stimulation of the region clorso- lateral from the facial nucleus, and sometimes from the caudal end of the nucleus also. In no case could we observe any move- ment of the facial muscles 011 the opposite side. The partial paralysis of facial muscles after lesions of the nucleus corre- sponded with the stimulation experiments, as auricular paral- ysis was noticed after medial lesions, paralysis of the orbicularis oculi in lateral lesions and that of the lips a i d the nostrils after anterior lesions.

Stimulation experiments were not exact enough to give R

clear localization of the facial muscles in their motor nucleus. Degeneration experiments give more precise results. In table 1, the degree of degeneration after lesions in different parts of the facial nucleus is given for the main facial muscles, or regions. The symbol ++++ indicates a degeneration of iiearlp 100% of motor fibers and end-plates, +++ of about 7570, ++ 50% degenerated end-plates, and tlie symbol + means about 2.5% of the end-plates degenerated; f indicates few degenerated fibers to be seen in the preparations.

From this table we may infer the location of ganglion cells which scpplp the different muscles (fig. 3 ) .

TA

BlJ

E 1

Deg

ree

of degcnerntion a

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of

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faci

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ird

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~

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____

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__

._

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-_

PO

SIT

ION

OF L

RSI

ON

IN F

AC

IAb

NUCLEUS

Lat

eral

A

nter

ior

Pos

teri

or

Infe

rior

T

otal

lesi

on

--_

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-_

__

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-

--

-

Plat

ysm

a ++

++

+ ++

+ ++

++

++

-

t.3

CI

CO

Styl

ohyo

id

Dig

astr

ic p

ost.

hell

y

Ant

erio

r au

rciu

lar

nius

rlcs

Supe

rior

aur

icul

ar m

vsvl

es

Pos

teri

or a

uric

ular

mus

cles

+++ -

+ -

+ -1-

+ ++

+ -

++++

++ + -

0 8

++++

-

++

-

-

Infe

rior

aur

icul

ar m

uscl

es

++++

fr

ont,

{ o

ceip

. O

ccip

itof r

onta

lis

-

++++

-

+

-

+++

++++

L

++

+++

++++

-

+++

-

++++

++

+ +

++

++++

+

++++

-

+

++++

++

++

+++t

Orh

irul

aris

oau

li -

Nas

al m

usrl

es

-

+++t

+++

-

Mus

cles

of

uppe

r li

p -

+++

++++

-

Mus

cles

of

low

er l

ip

++

+ ++

+ R

ucci

nato

r +

+ ++

+ 2

-

-

-

REPRESENTATION O F FACIAL MUSCLES 213

The ganglion cells for the platysma are located on the medial edge of the facial nucleus, in its caudal part. In 2 of our cases (nos. 9 and 15) we got tangential lesions which de- stroyed only a small strip on the medial edge, associated with

Fig. 3 Cross sections through the brain stem. A. anterior, B. intermediate and C. posterior level of the facial nucleus with indication of facial muscles repre- sented in different parts of it. r.d.V., radix descendens nervi trigemini; o.s., oliva superior.

214 JOHN SZENT~GOTHAI

almost complete degeneration in the platysma. K e fouiid also some evidence for the assumption that anterior parts of the platysma are supplied by anterior, posterior parts by poste- rior ganglion cells.

The ganglion cells wliich supply the styloliyoid muscle are situated in the posterior part of tlie nucleus dorsally and ni edially .

The posterior belly of the digastric showed no degeneration even in a case (no. 18) in which the whole nucleus was de- stroyed. From this we had to draw the conclusion that the ganglion cells f o r this muscle lie outside of the facial nucleus, probably in the accessory nucleus which lies between the facial and abclucent nuclei. In 2 cases (nos. 5 and 20), the lesion was placed just between these 2 nuclei, resulting in nearly complete degeneration in the posterior belly of the digastric. Several authors do not believe in the existence of an acces- sory facial nucleus in cats, but considering the small size of the posterior belly and its limited innervation in this animal we may suppose that a few scattered cells were enough to supply this muscle.

The field of the auricular muscles in the facial nucleus is of considcrable extent. Most of its ganglion cells lie in the medial half of the nucleus; a few are situated in the infclrior part of it. The localization of the anterior auricular muscles is anterior and lateral to the others. The superior auricular muscles are innervated by cells of the inferior part of the nucleus ; the most dorsal (clorsomedial) part of the nucleus supplies the posterior and inferior aurciular muscles. The great extent of the auriculomotor field in the facial nucleus is associated with the fact that the ear muscles of the cat are of large size, with rich innervation and highly developed function.

The scalp muscles are represented in the lateral half of the nucleus and in its inferior par t ; the frontalis anterior to tlie occipit alis.

The orbicularis and other eye-lid muscles are localized in the lateral pa r j of the nucleus, anterior and dorsal to the areas for the scalp muscles.

REPRESEATTATION O F FACIAL NV'SCLES 215

The of the upper

nasal and oral facial nucleus.

lip muscles are

muscles a re supplied by the oral pole The motor cells supplying nasal and

located rather ventrolaterally, those to the lower lip and mental muscles dorsomedially in this par t of the nucleus.

DISCUSSION

Comparing oiir observations with the results of earlier authors, as vaii Geliuchten (1898), Marinesco (1899), Parhon and Minea ( '07) and Papez ('27) who have studied the chro- matic changes in the nucleus of the facial nerve in the cat and other animals after extirpation of various branches of that nerve or various facial muscles, we may state that in some cases there is agreement, in others not. While our results do not agree with those of the earlier authors, in many respects there is substantial agreement with the findings of Papez ( '27). The 2 series of experiments a re in agreement as to the nieclial location of the cells supplying the platysma and the dorsomedial represent ation of the auricular muscles which are supplied by the posterior auricular nerve, as well as the lateral localization of the orbital and nsal muscles. I n other respects our findings differ from the previous results, e.g., in the question of dorsoventral and anteroposterior localizatioii and the significance of the accessory f ac id nucleus.

Our most important results may be explained as follows : 1. The lateral localization of the muscles around the eye

and perhaps also that of the nasal and frontal muscles may be due to neurobiotasis. The dominant source of iinpulses for these muscles is doubtless the spinal tract of the trigeininal nerve (e.g. conjunctival and corneal reflexes). If the migration of facial motor neurons is due to neurobiotasis, there is rea- son euougli for niuscles around the eye to take position on the lateral side of the nucleus very close to the spinal tract of the trigemhius. The platysma and auricular muscles have no im- portant reflex connections with the trigeininal system, hence the medial position of their cells of origin may be understood.

2. Concerning the anteroposterior localization, i t is of in- terest to note that muscles around the mouth and nostrils a re

216 JOHN SZENT~GOTHAI

represented in the oral pole of the nucleus, and the greater distance of a muscle from this area of the face, the more posterior is its representation in the facial nucleus. The situ- ation is very similar to the central representation of concentric zones of cutaneous sensibility in the descending trigeminal tract, as known from cases of syringobulbia. If we divide the face into concentric zones around the mouth and nostrils, the muscles of each zone are represented approximately in the same succession in &scs of the facial iiucleus divided by planes vertical to the axis of the brain stein (fig. 4). At first

Fig. 4 Diagram showing the representation (dorsorentral and nnterioposterior) of facial muscles, belonging t o different regions of the face, in the facial nucleus. o.s., oliva superior ; nu.VII., facial nucleus.

sight, it seems surprising that the facial muscles with their intricate pattern should be localized in such simple manner in their nucleus, but, comparing our results with the findings of Futamura ('06) on the early development of facial muscles, we see that the primary platysma, from which most of the facial muscles originate, lies in a concentric zone around the mouth and nostrils. Figure 5 shows an early stage of the development of the primary platpsma after Futamura. By later migrations of muscles this relation is naturally confused, but still manifest in the adult.

BEPKESE NTATION OF FACIAL MUSCLES 217

3. Most of the authors emphasized a dorsoventral localiza- tion because of the subdivisions of the facial nucleus into dorsal, intermediate and ventral groups. tTpper muscles on the face are gefierally believed to be supplied by the dorsal, lower situated muscles by the ventral, group. The dorso- ventral localization, was not very clear in our experiments because of technical difficulties. Because the roots of the facial nerve emerge from the dorsal side of the nucleus it was not possible to determine directly the muscles supplied by dorsal ganglion cells by placing lesions in the dorsal part of the nucleus. We therefore have to base our inference indirectly on the results after lesions in the ventral part of the nucleus. From these we may draw the conclusion, that muscles of the upper part of the head are generally supplied by ganglion cells of the ventral part of the nudeus while muscles of lower parts of the face are represented in the dorsal part (fig. 4). There are some exceptions to this rule, but these may be caused by migration of muscles in the later stages of development. 4. Neither in stinidation experiments nor by the degenera-

tion method were we able to obtain any evidence for a contra- lateral innervation of facial muscles often mentioned in the literature. The facial muscles have only a unilateral innerva- tion, as far as the nuclei are concerned.

5. The aberrant representation of the posterior belly of the digastric is to be explained perhaps by the fact that its ganglion cells of supply in the accessory nucleus are much closer to the motor trigeminal nucleus and approximately in similar position. It is understandable that 2 muscle bellies connected with each other on the periphery map also have some relation in their central representation. The situation would be very clear, if the anterior belly of the digastric were supplied by the posterior part of the motor trigeminal nu- cleus. I n that case we should have to consider the accessory facial nucleus as an aberrant part of the trigeminal, the roots of which join the facial nerve. From a series of experiments, which are beyond the scope of thiq paper, we unfortunately were forced to the conclusion that the anterior belly of the

218 JOHK S Z E N T ~ G O T H A I

digastricus aiid the inyloliyoid inuscle are supplied by the anterodorsal par t of the trigeininal nucleus.

6. Lastly we have to refer to the queatioii whether or not there is a relation between the representation of facial muscles aiid the various cell groups described hi the nucleus. It is ob- vious that there is a definite relation between the several muscles and the position of their motor ganglion cells in the nucleus, but we cannot identify the representation fields de- termiired by us either of single muscles or of larger muscle

Fig. 3 Platysma sheet of a humnii embryo in the sixth week of development. p.f., facial group ; p.o., occipital group; p c . , cervical plxtysma.

groups with any of the kiiowii cell groups of the nucleus. From this fact and other experience with cranial nuclei examined by the same method (oculoinotor, '41, ainbiguus, '43, and hypo- glossal, unpublished), we were coiiviiiced that the subdivisioiis of motor nnclei into different cell groups cannot be identified so simply with the representation of various muscles or muscle groups in the nucleus. We believe that authors often failed in exact determination of muscular localization because they tried to force an identification of muscular representation and nuclear subdivisions. The subdivision of motor nuclei

REPRESENTATIOS O F FACIAL MUSCLES 219

iiiay be due to many other factors of developmeiit (e.g. path- ways running through, etc.) which have nothing to do with the representation of iiiuscles within. Riigrations and other changes during the later developiiient of muscles are frequent, while the structure of the nuclei is determined rather early. A definite relation between cell clusters and muscular repre- seiitatioii may exist perhaps in earlier stages of development and may disappear later. Nevertheless we have to stress that there is a very strict localization for the ganglion cells tvliich supply every muscle in a certain part of the nucleus. The limits however between the fields of diff ereiit muscles within the nucleus are not sharp, a circuinstance which is also evi- dence against the identity of muscular representatioii and nuclear subdivisions. Our experiments show a considerable overlap of localization. There is nothing unusual in tliis re- sult, since overlap in central representation fields (e.g., motor cortex) appears in recent publications to be very coinnion in the central nervous system.

SUMMARY

With the aid of a modified stereotaxic instrument the nu- clear representation of facial and scalp niuscles was deter- iiiined on cats. Stimulation experiments were used for orientation. Small lesions were placed in different parts of the facial nucleus and subsequent traumatic degeneration of end- plates and motor fibers in different muscles was analyzed.

The nuclear representation of f acial muscles is as follows : Pla fy smo - medial edge of the nucleus. S f y l o h y o i d - dorsal and medial part of the posterior pole. Digrcstric pos t . belly - accessory facial nucleus. ,4 irricitlar ~ ~ 7 1 ~ s c k s - great field extending from clorsoniedial

Froiitulis - lateroveiitral part of the nucleus. Occipi fal is - lateroventral part, posterior to the frontalis. OrLicuZaris ocitli - most lateral part of the nucleus. Noscll and u p p e r l i p niii,sclrs - oral pole especially its latero-

Lower Zip rnicscles - oral pole especially its dorsomcdial part.

to internietlioventral.

ventral part.

220 JOHN SZEKTAGOTHAI

The muscles of concentric facial zones around the mouth and nostrils are represented in the same sequence in the anteroposterior direction in the facial nucleus. Muscles sup- plied by upper facial branches are represented in ventral parts of the nucleus, those supplied by lower branches in the dorsal part. The representation fields of different muscles and muscle groups show a considerable overlap.

LITERATURE CITED

BERNHEIMER, ST. 1897 Experimentelle Studien zur Kenntnis der Innemation der inneren und ausseren vom Oculomotorius versorgten Muskeln des Auges. Graefes Arch. f. Ophthalm., 44: 481-525.

FUTANURA, F. 1906 Ueber die Entwicklung der Fazialismuskulatur des Men- schen. Anat. Hefte, 50: 435-516.

GERUCRTEN, A. VAN L’origine du nerf facial ehez le lapin. Revue Xeurolo- gique, 6: 553.

HORSLEY, V., AND R. H. CLARKE The structure and functions of the cere- bellum examined by a new method. Brain, 32: 45-137.

MARINESCO, G. 1899 Nouvelles recherche8 sur l’origine du facial supbrieur et du facial infhrieur. La Presse MBdieale, 6 : 85-86.

PAPEZ, J. W. 1927 Subdirisions of the facial nucleus. J. Comp. Neur., 43: 159- 191.

PARHON, C. J., AND J. MIXEA 1907 L’origine du facial supbrieur. La Presse MBdieale, 15: 5”-52?.

SZENTAGOTHAI, .J. 1941 Die innere Gliederung des Oculomotoriuskerns. Brch. f . Psychiatr., 135: 127-135.

Die Lokalisation der Kehlkopfmusculatur in den Vaguskernen. Zeitschr. f . Anat., 112: 704-710.

Nervensgstem. Handb. d. Anat. d. Mensch., K. v. Bardeleben.

1898

1908

1943

ZIEHEN, TH. 1935 4: (Abt. 1-3).