Anatomy. - The oculomotor nucleus of the electric stargazers: Astro~ scopus guttatus and Astroseopus y~graecum. By C. U. ARIËNS KAPPERS.

(Communicated at the meeting of March 29. 1941.)

Through the kindness of Prof. U. DAHLGREN of Princeton University N. J. we received, some years ago, the brains of two very interesting fishes: Astroseopus guttatus and Astroscopus y~graecum, occurring on the S. E. coast of America aod in the Gulf of Mexico 1) .

As first observed by Dr. GILBERT for Astroscopus guttatus and by Or; HENSHALL for Astroscopus y~graecum these fishes produce an electric shock when touched. According to Miss WHITE chemical stimulation has the same effect. Dr. GILBERT found their e1ectric organs to be located behind the eyes 2). As described by Prof. DAHLGREN in Science 1906, in the Carnegie Institute publications of 1914 and in an article in the Ana~ tomische Anzeig'er of 1906 by DAHLG'REN and SILVESTER a large part of the eye muscles of these fishes has chaoged into an electric organ innervated by the oculomotor nerve.

Figure 1 is a copy of SILVESTER's drawing, showing on the right the extension of this organ aod on the left the external muscles of the sm all eye (the obliquus inferior is not visible in this aspect).

From thisdrawing it appears th at the muscles are very much reduced. The rectus inferior has even changed to a thin thread which only increases near its insertion on the eye balI.

All muscles, except the obliqui that have their insertions before the eye balI, are elongated to leave place for the e1ectric organ.

According to these authors and to Miss WHITE, who examined its ontogeneticdeve1opment the e1ectric organ derives its tissue from the myotomes of all the eye muscles except the rectus inferior and obliquus inferior.

Although the obliquus superior, innervated by the trochlear nerve, and the rectus extern us, innervated by the abducens, also participate in the structure of this organ, the organ, according to these authors, is innervated only by the oculomotor nerve by means of a strong branch, a small side~ branch of which innervates what is left of the rectus superior musc1e.

As appears from our copy of DAHLGREN'S and SILVESTER's picture and

1) We take this opportunity ta express our thanks ta Prof. DAHL(jREN for this rare material.

2) Quoted from DAHLGREN and SILVESTER (so also }ORDAN. A Guide ta the study of Fishes, New York 1905 and }ORDAN and EVERMANi" . The fishes of North and Middle America. Bull. U.S. National Museum No, 47) ,

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Erom our fig. 3 the oculomotor nerve is very big. lts transverse section is at least four times larger than that of the optic nerve.

Fig. I. Dorsal aspeet of Astroseopus y-graeewn, redrawn from DAHLGREN and SILVESTER. The m.m. obliqui of whlch only the m. obliquus superior is visible, are loeated frontally to the eleetrie organ, the extension of whieh is indieated on the right side. The m.m. reeti, originate behind the eleetrie organ. The reetus superior runs through the eleetrie organ and the reetus inferior is very much

reduced. Compare the relative sizes of the oculomotor and optie nerves.

Although the electric nerve leaves the bram with the branch innervating the rectus superior, it apparently contains fibres Erom the whole oculomotor nucleus, as already observed hy Miss WHITE.

Since the oculomotor nucleus of these fishes has not been described by these authors, we take this opportunity to give a brief description of its relations in Astroscopus guttatus and Astroscopus y~graecum. UnEortuna~ tely the state of preservation of the material. though quite sufficioot for stating the general relations. did not all ow us to study cytological details.

Our Eigure 2 shows the extension of 'the oculomotor nucleus of Astro~ scopus guttatus. projected on the sagittal plane of the brainstem. compared with an orclinary fish. Cottus scorpius. with normal eye muscles. From these diagrams. made in the way we introduced for measuring the locali~

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zation and extension of motor nuclei, it appears that the oeulomotor nucleus is enormously enlarged in Astroseopus guttatus. In Astroseopus y-graeeum its metric relations are about the same.

Astroscopus guttatus.

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Cottus scorpius.

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Fig. 2. Localization and sagittal extension of the eye muscIe nuclei and roots and of the motor trigeminus nucleus and root in Astroscopus guttatus. compared with those of a fish, Cottus scorpius, with ordinary eye muscles. The oculomotor nucleus and root are horizontal\y, the trochlear nucleus and root vertically striped. The abducens nucleus is indicated by concentric circles, the motor trigeminus

nucleus and root are dotted.

The oculomotor nucleus of Te1eosts may bedivided into a dorso-Iateral and a ventral part (HUET, KAPPERS, BLACK, VAN DER HORST, ADDENS).

The ventral part of the oeulomotor nucleus which, aeeording to HADI­DIAN's and DUNN's experiments on the Goldfish (Carassius auratus), innervates the reetus superior (and obliquus inferior) in our Astroseopi is less hypertrophied than the ,dorso-Iateral part.

From fig. 3 it appears that in Astroscopus guttatus the frontal pole of the dorso-Iateral nucleus protrudes forward into the optie ventricle, its middle part lies between the valvula eerebelli, (val. eer.) and the nucleus lateralis valvulae (N.L.V.), and its hindpole lies above the sulcus limitans of the aquaeduet, oeeupying the same plaee as HERRICK'S seeondary gustatory nucleus does in other Teleosts, extending baekward as far as the beg inning of the motor tri gem in us nucleus (Nu. V). The hindpoles

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Fig. 3. Series of transverse sections of the oculomotor nucleus and trochlear region of Astroscopus guttatus.

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Fig . 4. Series of transverse sections of the oculomotor nucleus and trochiear region of Astroseopus Y-graecum.

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of the nuclei of both sides are separated on th is level by the dorsal extension of the aquaeduct.

In Astroscopus y~graecum (fig. 4) the hindpoles of the nuclei eoalesee in the midline (as the dorso~lateral nuclei do). both halves being separated only by a thin septum. Together they praetically fill up the whole aquae~ duet. which at th is spot is eonsiderably extended by this nuclear mass.

This different morphology of the hindpoles in Astroscopus guttatus and Astroseopus y~graeeum apparently influenees the course of the troehlear fibres. In Astroseopusguttatus they run medially to the hindpole of the nucleus close to the ventricle. In Astroseopus y-graeeum. they run laterally to the hindpole of the nucleus.

Although the troehlear roots are weil preserved and have about the same position and size of the troehlear root in other Teleosts. the state of fixation in the eentre of our material did not allow us to traee with eer~ tainty the origin of its fibres.

All we ean say is th at we have not been able to traee these fibres to a separate troehlear nucleus on the plaee where it usually oeeurs in Teleosts. i.e. on top of the fase. longitudinalis posterior. Although this may be due to the state of our material, the relations in Astroseopus y-graeeum suggest that the troehlear eells are located at the hindpole of the eleetrie nucleus anc th at their celltype differs little from the type of the eleetric eells. although the eells are somewhat smaller.

The troehlear root; however. is not hypertrophied. In Astroseopus y~ graeeum it is even very smalI.

The abdueens is not hypertrophied either. perhaps it is evenredueed in size. The state of fixation not being any too good we have been able to find only one of its rootlets and by th is we loeated one group of ventral eells belonging to it. There may be. however. a seeond rootlet and group of eells. as in most T eleosts.

The large size of the oeulomotor nucleus is not due only to an inerease in number of its eells but ehiefly to their inerease in size. The eells themselves closely resembIe the eells of the eleetric nerves of Torpedo marmorata 1) described by BORCHERT. KApPERS. STUART and KAMp.

and Narke }aponiea 1). described by SUZUKl. They are hu ge multipolar eells. Whether there are plasmodesms between these eells. as described by SUZUKI in Narke }aponica. we do not know. Another point of resem~ blanee wirh the eleetric nucleus of the latter two fishes is its abundant vaseularisation. N early eaeh eell is loeated in a framework of capillaries 2).

There are two questions which have to be eonsidered in connection with ()ur subject.

1) The electric organ of these fishes is. however, derived from the gill musculature and innervated by the VII, IX and X nerves.

2) This is especially evident in our series of Astroscopus y-graecum, where the blood­vessels are still filled with blood. In our drawings only the larger bloodvessels are indicated.

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The first question concerns those eells of the oeulomotor nucleus th at do not innervate the eleetric organ but the oeulomotor muscles themselves. i.e. all the root eells of the reetus inferior and obliquus inferior (muscles whieh do not participate in building up the eleetric organ) and those root eells of the reetus superior and reetus intern us. that send their neurites into these muscles.

The reetus inferior muscIe being strongly redueed (see fig. 1). the seareh for its root eells (which in the goldfish are ehiefly loeated in the dorso­lateral nucleus) is like looking for a needie in a bottle of hay. The root eells of the 'more developed obliquus inferior muscIe aeeording to HADIDIAN's and DUNN'S experiments oeeur ehiefly in the ventral nucleus. It may be therefore. that tlie somewhat smaller and darker eells of the ventral nucleus. indicated in our mierophotograph of Astroscopus y-graecum (fig. 5). inner­vate this muscIe. Since. however. most eells of the reetus superior and about

bl,v.

b v.

Fig. 5. Transverse section about the middle of the oculomotor nucleus of Astroscopus y-graecum. Nu. 111 d.l. = dorso-Iateral. nu. 111 V = ventral part of

the nucleus; bI. v. = bloodvessels.

Proc. Ned. Akad. v. Wetensch., Amsterdam, Vol. XLIV, 1941. 25

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half of the eells of reetus internus aeeording to these authors are also located in the ventral nucleus, the somewhat smaller cells located here may as well serve the rectus superior and intern us.

Curiously enough the purely motor cells of the 111 nucleus are also larger than the III cells of an ordinary T eleost and the same may hold good Eor the cells of the trochlear nucleus, if our assumption that the latter are located at the hindpole of the electric nucleus is right.

Considering the general reduction of the eye muscles it is not astonishing that the number of these purely motor cells is smalI.

The second question is inspired by the fact that, whereas the myotomes of the trochlear and abducens muscles participate in the formation of the electric organ, the trochlear and abducens 'nerve ,do not participate in its innervation. Apparently the elements derived from the obliquus superior and rectus externus myotomes joining the electric organ are innervated by oculomotor branches.

This heterogenous innervation might be explained by an overlapping of the term in at ion of the three eye muscle tllerves.

Anastomoses of oculomotor fibres with the trochlear and abdueens ending in the obliquus superior and rectus externus muscles have been described by POIRIER and CHARPY for man. MURAT and RUPASSOW experi~ mentally confirmed their oceurrence in eats. This overlapping, which only implies a few fibres, may be compared with the plurisegmental innervation of extremity muscles experimentally proved by AODUHR and confirmed by LAwRENTJEW.

Another explanation, advocated by ADDENS, is based upon the pheno­menon of secondary heterotopic innervation, as also observed in the tail muscula'ture, where myotomes may be innervated ~y a root different from the root normally innervating that myotome.

Since peripheral anastomoses between the eye muscle nerves of Teleosts have not been observed, the latter explanation seems the more likely one.

LITERATURE.

ADDENS, The motor nuclei and roots of the cranial and first spinal nerves of Vertebrates. Zeitschr. f. d. ges. Anat., Bnd. 101. 1933.

AODUHR, Morphologischer Beweis der doppelten (plurisegmentalen) motorischen Inner­vation der einzelnen quergestreiften Muskeln bei Säugetieren. Anat. Anz .. Bnd. 49, 1916.

-----, Ueber die plurisegmentale Innervation der einzelnen quergestreiften Muskelfasem. Anat. Anz., Bnd. 52, 1919.

BLACK, The motor nuclei in phylogeny. A study of the phenomena of Neurobiotaxis 1. Cyclostomi and Pisces. Joum. Comp. Neur., Vol. 27, 1916---'17.

BORCHERT, Zur Kenntnis des Centralnervensystems von Torpedo, Jena 1903. Idem (2te Mitt.) Morpholog. Jahrb., Bnd. 36, 1906.

DAHLOREN, A new t;ype of electric organ in an American Teleost fish Astroscopus (Brevoort) Science, Vol. 23, 1906.

-----. The habit of Astroscopus and the development of its electric organs. Camegie Instit. Washington Publ. No. 183, 1914.

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DAHLGREN and SILVESTER, The electric organ of the stargazer Astroscopus (Breevoort). Anat. Anz. Bnd. 29, 1906.

HADIDIAN and DUNN, Localization in the oculomotor nuclei of the Goldfish. Journ. Comp. Neur., Vol. 68, 1938.

HERRICK, The central gustatory paths in the brain of bony fishes. Journ. Comp. Neur., Vol. 15, 1905.

HORST, VAN DER, De motorische kernen en banen in de hersenen der visschen, hare taxonomische waarde en neurobiotaktische beteekenis. Dissertatie, Amster­dam, 1916.

HUET, Notes on the trochlear and oculomotor nuclei and the trochlear root in lower Vertebrates. Proe. Kon. Akad. v. Wetensch., Amsterdam, 1911.

KAPPERS, ARIËNS, Weitere Mitteilungen über Neurobiotaxis VII. Die phylogenetische Entwicklung der motorisch en Wurzelkerne in Oblongata und Mittelhirn. Folia Neuro-biol.. Bnd. 6, 1912.

LA WRENTjEW, Studien über den feineren Bau der Nervenendigungen in der quergestreif. ten Muskulatur des Frosches 11. Ueber die plurisegmentelle Innervation der Muskelfasern. Zeitschr. mikro Anat. Forschung, Bnd. H, 1925.

MURAT und RUPASSOW, Ueber die plurisegmentelle Innervation der quergestreiften Muskeln des Katzenauges. Anat. Anz., Bnd. 84, 1937.

STUART and KAMP, The electric organ and its centres in Torpedo marmorata. Proc. Kon. Akad. v. Wetensch., Amsterdam, Vol. 37, 1934.

POIRIER et CHARPY, Traité d'anatomie humaine, T. 3, Paris 1904. SUZUKI, On the lob us electricus and the nervi electrici in Narko Japonica. Journ. of

oriental medicine, Vol. 25, 1936. WHITE, The origin of the electric organ in Astroscopus guttatus. Carnegie Instit.

Washington, publ. 252, 1918.

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