Exp. Brain Res. 23, 167 179 (1975) 9 by Springer-Verlag 1975
Trigeminal Representations of the Masticatory and Extraocular Proprioeeptors as Revealed by Horseradish Peroxidase Retrograde Transport M.R. Alvarado-Mallart, C. Batini, C. Buisseret-Delmas and J. Corvisier Laboratoire de Psyehophysiologie Sensorielle, Universit~ Paris VI Laboratoire d'Anatomie Compar6e, Universit~ Paris VII Laboratoire de Physiologic G6n4rale, Universi~6 Paris XI (France) Received May 15, I975 Summary. Horseradish peroxidase has been injected in the masticatory and extraocular muscles in newborn and adult cats to identify the cells of origin for the muscle endings. Labeled motoneurons in the nuclei of the I I I , IV, V and VI nerves have been observed. They are the parent cells of the motor terminals taking up the enzyme in the muscle injected. Labeled ganglionic cells have been found scattered all along the ipsilateral mesencephalic nucleus of the V nerve after injection of both the jaw closing and the jaw opening muscles. Labeled cells have also been found in the ipsilateral caudal part of the same nucleus after injection of the extraocular muscles. These results are interpreted as due to enzyme uptake by the sensory endings of the muscle studied. Moreover cell bodies in the semilunar ganglion were found marked for both groups of muscles injected showing a second ganglionic representation for the sensory endings. Key words: Masticatory muscles - - Extraoeular nucleus - - Semilunar ganglion
muscles - -
Mesencephalic
Introduction The mesencephalic nucleus of the V nerve (Mes V) was shown by Johnston (1909) to contain centrally displaced ganglionic cells. These cells are considered to be associated with the proprioceptors of the head region (Cajal, 1909). I n particular, first order neurons of the proprioeeptive afferents from certain jaw closing masticatory muscles have been identified in the Mes V of the cat (Corbin and Harrison, 1940; Jerge, 1963; Taylor and Davey, 1968; Cody et al., 1972). On the contrary no such connections have been shown for the jaw opening muscles which are considered to have only poor or atypical sensory innervation (Kidokoro et al., 1968; Sauerland and Thiele, 1970; Cody et al., 1972). much debated also is the presence in Mes V of the first order cells associated with the extraoeular eye muscle proprioceptors (Fillenz, I955; Cooper and Fillenz, 1955 ; Manni et al., 1966, 1968 ; see also Hosokawa, 1961) which have in eat atypical sensory innervation (Fillenz, 1955).
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g e c e n t l y however labeled cells have been observed i n the Mes V after injection of Horseradish Peroxidase ( I t R P ) in the rectus lateralis muscle (Alvarado-Mallal~ et al., 1975). U p t a k e a n d retrograde axonal t r a n s p o r t of HP~P has been repeatedly demonstrated in both, peripheral nerves (Kristensson a n d Olsson, 1971; K r i s t e n s s o n et al., 1971; Lavail a n d Lavail, 1972; Warr, 1973; K r i s t e n s s o n a n d Olsson, 1974; B u n t et al., 1974) a n d central fiber systems (Kuypers et al., 1974; N a u t a et al., 1974; Graybiel a n d Hartwieg, 1974). The results described b y AlvaradoMallart et al. (1975) d e m o n s t r a t e the possibility of using the enzyme to identify the cells of origin of muscle sensory endings. U p t a k e s of H R P at the t e r m i n a l a n d its s u b s e q u e n t retrograde axonal t r a n s p o r t have been used in the present work to d e t e r m i n e : t h a t the Mes V contains the ganglionic cells for the proprioceptors of b o t h the jaw opening a n d closing muscles; t h a t the Mes V contains the ganglionic cells for the proprioceptors of the extraocular muscles i n n e r v a t e d b y the I I I a n d I V nerves as well as b y the VI nerve. I n addition, the semilunar ganglion has also been explored as a possible location of first order n e u r o n s related to m a s t i c a t o r y a n d extraoeular sensory terminals.
Methods The experimental data have been obtained from 12 adult and 10 young eats (1--8 weeks of age). All animals were anesthetized with pentobarbital injected intraperitoneally (40 mg/kg in the adults and 15 mg/kg in the youngs). The following muscles have been treated with the HI, P: 1. Mastieatory Muscles: Temporalis, masseter, pterygoideus lateralis and mediMis, the jaw closing and the anterior belly of the digastrieus and the mylohyoideus, the jaw opening. 2. Extraoeular Muscles: Rectus superior, inferior, medialis and obliqnus inferior innervated by the oeulomotor nerve (n III); the obliquus superior innervated by the troehlear (n IV) and the rectus lateralis innervated by the abducens (n VI). Before injection of the enzyme the mastieatory as well as the extraoenlar muscles were sufficiently dissected in situ to be separated from the surrounding tissues and muscles. The nerves to the ipsilateral masseter, digastricus and mylohyoideus muscles were severed before injecting the pterygoideus medialis in order to prevent diffusion of the enzyme to the neighbouring muscles. In two eases the maxillary and the mandibular divisions of the trigeminal nerve were severed before injecting the eye muscles. Doses of 5--40/A of HRP (Sigma VI) at 10--25~ in Ringer solution were used for each muscle according to their size. The injections were performed unilaterally or bilaterally using a hamilton mierosiringe. The tracer was introduced at several points inside the muscle so that it could be taken up by a maximum number of terminals. In 3 control experiments for both mastieatory and extraocular muscles, the tracer was deliberately deposited outside the muscles in contact with their surface to ascertain that marked cells in Mes V were not due to leaking of the enzyme to the surrounding tissues. Survival times of 24--75 hours were allowed to permit the retrograde transport of the exogenous peroxidase to the cells bodies (Kristensson et al., 1971; Bunt et al., I974). Two animals, not injected were used as control, to cheek that no endogenous peroxidase was present in the nervous structures examined. All the animals were perfused with a fixative solution (1% glutarMdehyde; 2.5% paraformaldehyde; 0.2O/o CaCe2 in 0.13/I S6erensen buffer at pH 7.6). The brain stem and the semilunar ganglion corresponding to the side injected were removed and placed in the perfusion solution for 3--12 hours, then washed in 0.1M phosphate buffer containing 30% sucrose.
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Frozen sections, 40 /l thick, of the brainstem and ganglion were cut and serially placed in individual containers and preincubated for 20--30 rain at 40~ in a solution of 0.1M tris buffer (pH 7.6). I-Iydrogene peroxid was added, incubated for another 20--30 rain at room temperature, then washed in SSerensen buffer and distilled water. The sections were finally moun~ed on slides and lightly s~ained with 1% cresylviolet.
Results The positive findings observed in the experiments carried out on new born animals were similar to those obtained in the adults. They will be described together. As a consequence of the injection of t I R P in the masticatory as well as in the extraocular muscles, three groups of cells were found labeled after the histochemical reaction: i) the motoneurons corresponding to the motor endings of the muscles, ii) ganglionic cells in the Mes V and iii) ganglionic cells in the semilunar ganglion.
Marking the Motoneurons As first described by Kristensson and Olsson (1971), the I-II~P injected in a muscle is taken up by the motor terminals and transported through the axons to the parent motoneurons which accumulate the I-IRP. Thus the histoehemical reaction serves as a method to identify, in a given motor nucleus, the group of cells innervating a single muscle. This localization has been described elsewere for the masticatory (Batini et al., 1975) as well as for the extraocular muscles (Gacek, 1974) and will not be considered here in detail. Since the localization of the motoneurons for the extraoeular muscles is well established, we have used the labeling of motoneurons in specific nuclei as a control for the fact that an injection of I-IRP in a particular extraocnlar muscle had indeed been confined to that muscle. I f the H R P had diffused to another muscle, motoneurons should have been marked in appropriate parent nucleus. As pointed out before (Alvarado-Mallart et al., 1975), such diffusion could be observed in some cases (in particular when the experiments were carried out in newborn animals) due to the small volume of extraoeular muscles and to their very close proximity inside the orbital cavity. Experiments in which spread of the enzyme into other non injected extraoeular muscles was indicated by marked motoneurons have also been taken into consideration for marked ganglionic cells. One to four of the muscles innervated by the I I I nerve have been injected simultaneously and the results were considered positive when labeled motoneurons were found in the corresponding I I I nucleus only. The obliquus inferior and the rectus laterMis were individually injected and results were considered localized when the contralateral IV nucleus or the ipsilateral VI nucleus only were respectively labeled. Figure 1 gives an example of marked cells in the trochlear nucleus. The mastieatory muscles were always injected individually. Since their motoneurons are all located in the motor nucleus of the V nerve it would be difficult to detect peripheral diffusion of Ht~P by their position in the nucleus. The larger size and accessibility of these muscles permitted visual control of the extent of spread of the injected enzyme. When needed the nerves entering the neighbouring muscles were severed (see Methods).
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Fig. 1. Labeled motoneurons after injection of HRP in the obliquus superior muscle. (A) Micrograph of the nuclei of the IV nerve showing that only cells of the contralateral nucleus are marked (right). (B) Some of the labeled motoneurons seen in A at higher magnification. The granular appearance of the HRP deposits, as seen in these cells, is the criterion for a positive result
Mar/sing Ganglionic Cells o/the Me~encephalic Nucleus o/the V Nerve I n the first experiments only, unilateral injections have been made for the masticatory as well as for the extraoeular muscles. As expected (Corbin, 1940; Jerge, 1963), in all eases positive results weie obtained only in the ipsilateral meseneephalic nucleus. Therefore in subsequent experiments, both sides have been used in the same animal. The lesults to be described are all considered us being strictly unilateral. After injection of each of the jaw closing muscles, a number of ganglionic cells in Mes V have shown typical brown granules in their soma. Figure 2A and B shows some specimens of these neurons. For the masseter muscle, the marked ganglionic cells were found uniformely distributed within the nucleus with no sign of localization. Similarly, those from the temporalis were found throughout the nucleus although a higher density of labeled ceils was found in its anterior part. These results are in agreement with previous physiological findings (Cody et al., 1972). For the pterygoidei muscles, labeled cells in Mes V have been found by iniecting not only the medialis, but also the lateralis. Here again a smaller number of scattered neurons could be traced from the anterior to the posterior part of the nucleus. After injection of the enzyme in each of the two jaw opening muscles, the anterior belly of the digastrieus and the mylohyoideus, a few ganglionic cells in Nes V have shown also the typical positive reaction (Fig. 2C). I n these eases the scattered labeled neurons were found only in the posterior half of the nucleus. As stated before, the extraoeular muscles have been considered for injection of Ht~P in three groups according to their motor innervation by the I I I , IV and VI nerves in order to establish possible differences in the loeMization of the first order sensory neurons. However the localization have shown a remarkable consisteney so that they can be described together. Labeled cells were found in Mes V
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Fig. 2. Labeled ganglionic cells in Mes V after injection of HRP in the masticatory muscles. Examples of a positive reaction in cells following injection of the masseter (A), the pterygoideus l~teralis (B) and the mylohyoideus (C). Arrows in B and C point to marked cells shown at higher magnification in the insets (Fig. 3) when diffusion of the enzyme to n e i g h b o u r i n g extraoeular muscles was k n o w n to occur a n d when the enzyme was k n o w n to be confined to the muscle injected. The m a r k e d cells i n Mes V were scattered i n the posterior half of the
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Fig. 3. Labeled ganglionic cells in Mes V after injection of HI~P in the extraocular muscles. (A) The 4 muscles innervated b y the I I I nerve were injected after section of the maxillary and the mandibular division of the V nerve. (B) A view of the lateral part of the velum medullaris anterior showing 3 marked cells (arrows a, b, c) one of which (c) is shown at higher magnification. I n this case the enzyme was injected in the rectus lateralis b u t diffusion h a d occurred into the muscles innervated by the I I I nerve. (C) Injection in the obliquus superior nucleus. However, when considered together the extraocular muscles appeared to be more densely represented in the posterior third of the nucleus. In addition few
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Fig. 4. Marked cells distribution ill Mes V. Marked cell distributions in the frontal sections examined are sehematicMly presented as degrees of shading on a vertical projection of the Mes V. The vertical plane outline of Mes V is obtained from the cat stereotaxic atlas (Berman, 1968). M2g mastieatory museles show a uniform distribution, EOM the extraoeular muscles are largely represented in the posterior third of the nucleus
cells were f o u n d l a b e l e d in t h e l a t e r a l p a r t of t h e l a m i n a m e d u l l a r i s anterior, a n e x t e n s i o n of t h e Mes V (Pearson, 1949). I t is interesting to n o t e t h a t ganglionic cells h a v e never been f o u n d in this position when t h e t r a c e r was i n j e c t e d in t h e m a s t i c a t o r y muscles. These findings clearly establish t h a t first order neurons of t h e sensory t e r m i n a l s for all t h e m a s t i c a t o r y a n d e x t r a o e u l a r muscles here e x a m i n e d , are indeed represented in t h e Mes V of t h e eat. Since t h e sensory fibers are carried r e s p e c t i v e l y b y t h e m a n d i b u l a r (Johnston, i909) a n d t h e o p h t h a l m i c division (Batini et al., 1975) of t h e trigeminM nerve, t h e d i s t r i b u t i o n of ganglionic cells r e l a t e d to m a s t i c a t o r y a n d to e x t r a o c u l a r muscles has been m a p p e d in Mes V as shown in Fig. 4. I t is possible t h a t n o t all t h e sensory endings t a k e u p H R P due to t h e localized injections. Thus t h e n u m b e r s of m a r k e d cells in each e x p e r i m e n t c a n n o t be con-
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Fig. 5. Marked ganglionic cells in the semilunar ganglion after injection of HRP in the mastieatery (A) and ~he extraocular (B) muscles
sidered as representing all the sensory endings in a muscle. With the exception of the two large muscles, the masseter and temporMis, marked cells in Mes V rarely exceeded ten units per muscle. I f these are the real quantities~ it may be difficult to attribute a functional meaning to this group of cells. We therefore examined the problem by comparison with previous data. The ganglionic representation of the masseter and temporalis is anatomically well established (Thelander, i924; Corbin, 1940) and its function has been repeatedly demonstrated (Corbin and Harrison, 1940; Jerge, 1963 ; Taylor and Davey, 1968 ; ttugelin and Bonvallet, 1957 ; Cody et al., 1972; Cooper et al., 1953). I n particular Dault and Smith (1969) after section of the ipsilateral masseterie nerve, counted 107--227 chromatolytic cells in Mes V. with the masseter. Therefore it appears that only part of the sensory endings in a muscle take up the enzyme. The same authors also pointed out that the temporalis is relatively less represented considering its larger weight. By reference to their relative weight, as measured in one adult animal, we also found that either the jaw closing or the jaw opening muscles were less represented than the masseter, while the situation was reversed for the extraocular muscles. The present experiments cannot exclude the possibility of a greater uptake of the enzyme in the smaller muscles and/or differences in uptake due to a ~n~r~i~nl~.r . . . . . . . . . . . mnrnhnlna~T~ . . . . . . . . ~J nf . . . t. h~ .. receptors.
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Marking Ganglionic Cells o/the Semilunar Ganglion I t has been demonstrated (Szents 1948) for the masticatory jaw closing muscles t h a t the muscle spindles have their somata located in the Mes V while the tendon organs have their somata in the semilunar ganglion. This dual representation of the proprioeeption has been confirmed in our experiments and has been extended to all the masticatory muscles. Positive reactions have been found in cells of the ipsilateral semilunar ganglion as we]] as in Mes V for all the jaw closing and opening muscles (Fig. 5A). Labeled neurons in the ipsilateral ganglion have been found after injection of the three groups of extraocular muscles (Fig. 5B). However, in this case they might be the result of a partial leaking of the enzyme at the site of the injection. Therefore they could be interpreted as due to other trigeminal receptors rather than to muscle terminals. Nevertheless the control experiments (see later) indicate t h a t at least part of the positive reaction are due to receptors located in the muscle. Whether these receptors are tendinous or muscular is not possible to determine by the tracer method. H R P injection made in the region of the tendons also yields positive reactions. I n this respect it is worthwile to mention t h a t the obliquus superior muscle has shown up to 10 times more labeled cells in the ganglion than the other extraocular or small volume masticatory muscles. The distal tendon of the obliquus superior has a much greater surface area which extends through the trochlea.
Controls Control experiments have been performed in animals not injected with H R P but submitted to the same histochemieal procedure. No marked cells could be found in the brainstem and the semilunar ganglion, indicating an absence of endogenous peroxidase in the structure analysed. I n other controls, HI~P was deposited at the surface of the muscles (see Methods) in order to check for diffusion of the tracer to other ophthalmic or mandibular terminals. No positive reaction has been found in the Mes V. A single labeled cell could be traced in the semilunar ganglion in one animal after injecting within the orbital cavity and none for the masticatory muscles. Finally in other experiments complete sections of the maxillary and the mandibular division (including the motor branch) of the trigeminal nerve were performed before injecting the eye muscles to prevent transport by terminals other than those of the ophthalmic nerve. I n fact the maxillary division carries the fibers from the periodontal pressure receptors (Pfaffmann, 1939) which have their cell bodies in the Mes V (Corbin and Harrison, 1940), while the mandibular division carries the sensory fibers from the masticatory muscles. As expected, in this case positive reactions have been observed in the Mes V (Fig. 3A) and in the semilunar ganglion. Discussion I t is generally accepted (see Hosokawa, 1961) t h a t the mesencephalic nucleus is connected with the sensory innervation of the masticatory muscles. However after lesions of the mesencephalic root, degeneration has been observed in fibers of the nerve to the jaw closing muscles, while no such degeneration could be detected in the jaw opening (Thelander, 1924; Szents 1948; Corbin, 1940).
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Similarly from a functional point of view stretch receptors of the jaw closing muscles only have been demonstrated to activate units of the Mes V (Corbin and Harrison, 1940; Harrison and Corbin, 1941; Jerge, 1963; Taylor and Davey, 1968; Smith, 1969; Cody et al., 1972) although Jerge (1963) could not find the projection of the pterygoideus lateralis. The problem of the representation of the extraocular muscles in Mes V is more debated. The positive results obtained by Freeman (1925) and Sheinin (1933) with the retrograde degeneration method are conflicting with later experiments by Corbin (1940). This author claims that he was unable to find degenerated fibers to the extraocular muscles after partial lesions of the Mes V nucleus and tract in cat. Functionally again, the primary projection from the extraoeular muscle stretch receptors described by some authors (Cooper et al., 1953, 1955; Fillenz, 1955; Buisseret et al., 1972 ; Alvarado-Mallart et aI., 1975) has not been found by others (Corbin and Harrison, 1940; Jerge, 1963, Cody et al., I972). In the present experiments we have been able to show that both groups of masticatory muscles as well as the extraocular muscles do have their sensory representation in the Mes V nucleus in eat. Of course, the method used here does not permit tracing the primary fibers, however, it permits positive identification of the neurons. In the ease of the degeneration method, an absence of results might be less reliable, in particular in view of the difficulty of completely destroying the mesencephalic tract. Partial lesions would not be effective due to the large distribution of the corresponding cells in the nucleus. On the other hand, one has to consider that the cell bodies corresponding to a single muscle are largely scattered and few in nmnber (at least for the small volume muscles) in a nucleus which is mostly formed by a unicellular layer for a length of 8 ram. Therefore they might be difficult to detect by a mieroelectrode sampling. This might explain why the physiological experiments mostly deal with neurons related to the masseter and temporalis. Several authors have postulated a proprioceptive representation in the semilunar ganglion when tendineous receptors in the masticatory muscles failed to show their primary neurons in Mes V (Szents 1948; Jerge, 1963; Taylor and Davey, i968; Cody et al., 1972). Manni et al. (1966, 1968) found, in Gasser's ganglion, ceils activated by stretching the extraoeular muscles in the lamb and pig, but not in the eat. Our results have shown a clear second sensory representation in this ganglion for both the jaw closing and law opening and possibly for the extraoeular muscles. Muscle spindles and tendon organs in the jaw closing muscles have been reported (see I-Iosokawa, 1961). But the pterygoideus lateralis failed to show any muscle spindles (Freimann, 1954; Smith Dale and Marearian, 1967). For the jaw opening muscles almost nothing is known; Baum (1900) found no muscle spindles in either belly of the digastrieus while Gregor (1903) described them in the mylohyoideus. Tendon (Huber, 1900) and muscle receptors in the extraoeular muscles have been described (see Cooper, Daniel and Whitteridge, 1955; Bach-y-Rita, 1971). However in cat, the typical muscle spindles are absent although freely ending stretch sensitive afferents have been reported (Fillenz, 1955; Baeh-y-gita and Ito, i966; Buisseret et al., 1972; Batini et al., 1974). I t is possible that in searching histologically for a particular receptor like the muscle spindle, atypical sensory endings
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could be missed, b u t could be d e m o n s t r a t e d b y a f u n c t i o n a l experiment. The results reported here clearly indicate the presence of sensory t e r m i n a l s in each of the muscles examined. H R P has n o t been d e m o n s t r a t e d to be selectively t a k e n up b y a n y p a r t i c u l a r terminal, t h u s no conclusions m a y be d r a w n regarding the exact n a t u r e of the sensory endings which took u p the m a r k e r w i t h i n the muscles. SzentAgothai (1948) has d e m o n s t r a t e d t h a t for the jaw closing muscles, the p r i m a r y n e u r o n s for the muscle spindles are in the Mes V nucleus, while those of the t e n d o n organs are in the s e m i l u n a r g~nglion. I f the labeled p r i m a r y n e u r o n s i n the present s t u d y give rise to proprioeeptors, the results presented here suggest t h a t the same t y p e of double r e p r e s e n t a t i o n could be e x t e n d e d to the jaw opening as well as to the extraocular muscles.
Acknowledgements. The authors are indebted to Jacques Reperant for showing them the histochemical techniques, to Christiane Pages for her technical assistance and to Fran~oise Lanery for typing the manuscript. This work has been partially supported by "La Fondation pour la Recherche M6dicale Frangaise". References Alvarado-MMlart, M. R., Batini, C., Buisseret-Delmas, C., Gueritaud, J. P., Horcholle-Bossavit, G., Tyd-Dumont, S. : Mesoncephalie projections of the rectus laterMis muscle afferents in the cat. Arch. itM. Biol. 113, 1--20 (1975) Bach-y-Rita, P., Ire, F. : Properties of stretch receptors in cat extraoeular muscles. J. Physiol. (Lend.) 186, 663--688 (1966) Batini, C., Buisseret, P., Buisseret-Delmas, C." Trigeminal pathway of the extrinsic eye muscle afferents in cat. Brain Res. 85, 74--78 (1975) Batini, C., Buisseret, P., Kado, R.T.. Extraocular proprioeeptive and trigeminal projections to the Purkinje cells of the eerebellar cortex. Arch. ital. Biol. 112, 1--17 (1974) Batini, C., Buisseret-Delmas, C., Corvisier, J. : Capture et transport de la peroxydase exog~ne dans les muscles masticateurs. Localisation des motoneurones. C.R. Acad. Sci. (Paris) 280, 2239--2240 (1975) Baum, J." Beitr~ge zur Kenntnis der Muskelspindeln. Anat. Hefte, L. Aht. 13, 249--305 (1900) Buisseret, P., Gueritaud, G.P., Horcholle-Bossavit, G., Tyd-Dumont, S.: Projections m@senc@hMiques des aff6renees proprioceptives de la musculature extrins@que des yeux. J. Physiol. (Paris) 65, 369A (1972) Bunt, A.H., Lund, R.D., Lund, J. S. : l~etrogr~de axonal transport of horseradish peroxidase by ganglion cells of the albino rat retina. Brain Res. 73, 215--228 (1974) Cajal, S., RamSn y: Histologie du syst~me nerveux de l'homme et des Vert@br6s. T. II, 993 pp. Paris: Maloine 1911 Cody, F. W. J., Lee, 1%.W. It., Taylor, A. : A functional analysis of the components of the meseneephalic nucleus of the fifth nerve in the cat. J. Physiol. (Lend.) 226, 24~9--261 (1972) Cooper, S., Daniel, P.D., Whitteridge, D. : Nerve impulses in the brain stem of the goat. Short latency responses obtained by stretching the extrinsic eye muscles and the jaw muscles. J. Physiol. (Lend.) 120, 4~71~90 (1953) Cooper, S., Daniel, P.D., Whitteridge, D. : Muscle spindles and other sensory endings in the extrinsic eye muscles. The physiology and anatomy of these receptors and of their eonnexions with the brain stem. Brain 78, 564--583 (1955) Cooper, S., Fillenz, M. : Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of these muscles. J. :Physiol. (Lend.) 127, 400--413 (1955) Corbin, K.B.: Observations on the peripheral distribution of fibers arising in the mesencephMie nucleus of the fifth cranial nerve. J. comp. Neurol. 73, 153--177 (1940) Corbin, K.B., Harrison, F. : Function of meseneephalic root of fifth cranial nerve. J. Neurophysiol. 3, 423--435 (1940) 13 Exp.:Brainl~es. Vol. 23
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M. 1~. Alvarado-Mallart et al.
Dault, S. I-I., Smith, R.D. : A quantitative study of the nucleus of the mesencephalic tract of the trigeminal nerve of the cat. Anat. l~ec. 165, 79--87 (1969) Fillenz, 1Vi.: Responses in the brain stem of the eat to stretch of extrinsic ocular muscles. J. Physiol. (Lond.) 128, 182--189 (1955) Freeman, W.T.: The relationship of the radix mesencephalica trigemini to the extraocular muscles. Arch. Neurol. Psychiat. (Chic.) 14, 111--113 (1925) Friemann, 1%.: Untersuchungen fiber Zahl und Anordnung der Muskelspindeln in den Kaumuskeln des Menchen. Anat. Ariz. 100, 18--20 (1954) Gacek, R.g. : Localization of neurons supplying the extraocular muscles in the kitten using horseradish peroxidase. Exp. Neurol. 44, 3 8 1 4 0 3 (1974) Graybiel, A. ~., I-Iartwieg, E. A. : Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques. Brain Res. 81, 543--551 (1974) Gregor, A.: Ueber die Vertheilung der Muskelspindeln in der Muskulatur des Menschlichen FStus. Arch. Anat. Physiol., Abt. Jahrg., 112--196 (190r Harrison, F., Corbin, K.B.: The central pathway for the jaw-jerk. Amer. J. Physiol. 135, 4 3 9 ~ 4 5 (1941) Hosokawa, I-I.: Proprioeeptive innervation of striated muscles in the territory of cranial nerves. Tex. l%ep. Biol. Med. 19, 405--464 (1961) Huber, G.C. : Sensory nerve terminations in the tendons of the extrinsic eye muscles of the cat. J. comp. I~eurol. 10, 152--158 (1900) I-Iugelin, A., Bonvallet, M.: Tonus cortical et contrble de la facilitation motrice d'origine r6ticulaire. J. Physiol. (Paris) 49, 1171--1200 (1957) Jerge, C.R.: Organization and function of the trigeminal mesencephalic nucleus. J. Neurophysiol. 26, 379--382 (1963) Johnston, J.B.: The radix mesencephalica trigemini. J. comp. l~eurol. 19, 593--664 (1909) Kidokoro, Y., Kubota, K., Shuto, S., Sumino, R.: Reflex organization of cat masticatory muscles. J. Neurophysiol. 81, 695--708 (1968) Kristensson, K., Olsson, Y.: Retrograde axonal transport of protein. Brain Res. 29, 363--365 (1971) Kristensson, K., 01sson, Y.: Retrograde transport of horseradish peroxidase in transected axons. I. Time relationship between transport and induction of ehromatolysis. Brain Res. 79, 101--109 (1974) Kristensson, K., 01sson, Y., S]Sstrand, J.: Axonal uptake and retregrade transport of exogenous proteins in the hypoglossal nerve. Brain Res. 82, 3 9 9 4 0 6 (1971) Kuypers, H. G. J.M., Kievit, J., Groen-Klevant, A.C. : Retrograde axonal transport of horseradish peroxidase in rat's forebrain. Brain Res. 67, 211--218 (1974) Lavail, J.H., Lavail, M.M.: Retrograde axonal transport in the central nervous system. Science 176, 1416--1417 (1972) Manni, E., Bortolami, R., Desole, C. : Eye muscle proprioception and the semilunar ganglion. Exp. :Neurol. 16, 226--236 (1966) Manni, E., Bortolami, R., Desole, C. : Peripheral pathway of eye muscle proprioception. Exp. Neurol. 22, 1--12 (1968) Nauta, H.J.W., Pritz, M.B., Lasek, R.J.: Afferents to the rat caudoputamen studied with horseradish peroxidase. An evaluation of a retrograde neuroanatomical research method. Brain Res. 67, 219--238 (1974) Pearson, A.A.: Further observations on the mesencephalic root of the trigeminal nerve. J. comp. Neurol. 91, 147--194 (1949) Pfaffmann, C." Afferent impulses from the teeth due to pressure and noxious stimulation. J. Physiol. (Lond.) 97, 207--219 (1939) Sauerland, E.K., Thiele, H.: Presynaptic depolarization of lingual and glossopharyngeal nerve afferents induced by stimulation of trigeminal proprioeeptive fibers. Exp. I~eurol. 28, 344--355 (1970) Sheinin, J.J." Studies of the mesencephalic nucleus in the normal and experimental cat. Anat. Rec. 55, 36 (1933) Smith, P~.D. : Localization of the neurons innervating tendon spindles of masticatory muscles. Exp. Nenrol. 25, 646--655 (1969)
Mastieatory, Extraoeular Trigeminal Representation
179
Smith, R.D., Marearian, II.Q. : The neuromuscular spindles of the lateral pterygoid muscle. Anat. Anz. Bd. 120, 47--53 (1967) Szents J.." Anatomical considerations of monosynaptic reflex ares. J. Neurophysiol. 11, 445--454 (1948) Taylor, A., Davey, M. R. : Behaviour of jaw muscle stretch receptors during active and passive movements in eats. Nature (Lond.) 220, 301--302 (1968) Thelander, It. E. : The course and distribution of the radix meseneephaliea trigemini in the eat. J. eomp. Neurol. 37, 207--220 (1924) Wart, W.B.. Localization of olivocochlear neurons by means of retrograde axonal transport of horseradish peroxidase. Anat. Ree. 1"/5, 464 (1973) Dr. C. Batini Laboratoire de Psyehophysiologie Sensorielle Universitg Paris VI 9, Quai Saint Bernard F - 75005 Paris France
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