View source for Talk:Paper - The morphology and morphogenesis of the choroid plexuses with especial reference to the development of the lateral telencephalic plexus in Chrysemys marginata (1916)

===The Morphology And Morphogenesis Of The Choroid Plexuses With Especial Reference To The Development Of The Lateral Telencephalic Plexus In Chrysemys Marginata===

l'i;i{(I\AL MAILi:V From llic Aualoinirnl Lnlxunlni!/ of Die Xorthirrslrnt r>iii'crsilif Medical School^

TWKNTV-SKVKN FKiURES



(•(».\ii;Ni-s

Introduction 507

History 5f;S

Material and Methods . 519

Doscri|)tioii 520

Discussion 525

Conclusions . 528



IN ll{< (DICTION

111 ;i rectMit coiiiinuiiicataoii. llic aullun- ( I^ailcy, 'L')) presented an inteipietation of the latertil telenceplialie elioroid plexus in the human embryo based on ontoj:;enetie and pliylop;enetic evidenee. The phylog;enetie evidence ])resented consisted of the most accurate descriptions a\'aihible of the de\'elopment of this structure in the lower vertebrates, viz., Warren's ('05) account of Necturus maculatus and Tandler and Kant or 's ('07) account of Platydactylus mauritanicus. With a \'iew to confirming, and strengthening if possible, the phylogenetic evidence it was determined to in\'estigate more definitely the de^'elopment of the prosencephalic choroid plexuses in others of the lower vertebrates. The following scheme taken from Wilder was accepted

1 Contrihutioii No. JJ. Suhinittcd for publication July 20, 1916.

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5()S PEHCIVAL HAILKV

to represent as accui-ately as possible the phylogenetic stages of greatest value:

Ainphioxus

Cyclostoines

Selachians

Ganoids

Urodeles (for Stegocephali)

Chelonia (for Theromorphs)

Monotremes (for Pantatheria)

Marsupials (for primitive Insectivora)

Insectivora

Lemurs (modern Mesodonta)

Cercopithecoidae (tailed moniveys of Old World)

Tailless Apes (Gorilla, etc.)

Pithecanthropus (extinct)

Homo primigenius (extinct)

Homo sapiens

Below the Urodeles, the lateral telencephalic choroid plexus is very rudimentary if it appears at all. Its condition in the Urodeles has been thoroughly elucidated by Warren's ('05) account of Necturus maculatus. For the Chelonia, Chrysemys marginata was selected because it was readily accessible and also because a great part of the work had already been admirably done by Warren ('11) in the course of his investigation of the Paraphysis and Pineal Region in Reptilia." It stands a little closer to the line of ascent of the mammals than the hzard, Platydactylus mauritanicus, described by Tandler and Kantor. Of the forms above the Chelonia, only Didelphys virgin iana representing the Marsupials, was available. The present communication is concerned with Chrysemys marginata and a review of the literature, leaving Didelphys for a later paper.

HISTORY

There are no choroid plexuses in Amphioxus (Burckhardt, '94).

Ahlborn ('83) describes well developed plexuses in the roof of the hindbrain of Petromyzon planeri, and also in the roof of the midbrain. The plexus of the diencephalic roof is not so well developed and no reference is made to any telencephalic plexuses. Burckhardt ('94) writes of Petromyzon fluviatihs:



MORPHOGENESIS OF THE CHOROID PLEXUSES 509

Aiich hier wie bei Teleostiern bleiben die Plexus inferioris (median telencephalic choroid plexus) nur in Gestalt einer Querfalte nachweisbar, die Paraphyse ist eine blosse Kuppel, der caudalen Rand wir als rudinientares \'elum auffassen.

There are no lateral telencephalic choroid plexuses in Cyclostomes.

Among the Selachians, ho^ve^"er, there is a well formed plexus inferioris in Xotidanus according to Burckhardt ('94), but no lateral telencephalic plexuses appear. On the other hand, I infer from Kappers and Carpenter ('ID tliat in Chiniaera monstrosa the lateral plexuses are present.

Der ependyniale Theil der Sciiluszplatlc \V()ll»t sicli in ihiciii tVoiitalsten Al)schnitt ctwas iiber deni Niveau des (ieliinies hiuaus cine Art paraj)hyse darslt'ilciul uiu sicli daini plotzlieh wieder eiuzufalteii und in den unparen X'entrikel eindrinjicnd den plexus chorioideus vent rieuli imparis zu bildcn. wovon audi jicrinRe Auslaufci- in den schnialen Seit(MiventriUe!n ilvt^ (lehirns eindrinjien.

And Minot ('01) in dosciihing Acantliias lemarks:



verA



The velum has now distinctly the character of a choroid |ilcxus, beiu}!; _ry irregular in the form of its surface, rich in blood vessels, covered by a thin ependyma ami projecting far into the ca\'ity of the brain. Laterally the projections from its surface are much more developed and as the organ has grown forward alongside the median para])hysal arch, it has produced what we can now easily identify as the jilexus of the lateral ventricle. These i)lexuses are therefore to be interpicted morphologically as scH'ondary modifications or appendages of the primary velum transversum Attention should be jiaid to the

two lateral projections. L.ch., of the ependyma on the anterior sui-face of the velum, because these j^rojections not only fix the lateral boundaries of the paraphysal arch but also are the anlages of the choroid plexuses of the lateral ventricles. These anlages from this stage (28.0 mm.) on rapidly increase both in size and in comjilication of form.

D'Erchia ('9(3) shows in Torpedo the velum transformed into a plexus and the tela chorioidea diencephali practically nonexistent. In fact, this seems to be the tendency of these two structures in the entire Selachian group. There is a i)lexus in the roof of the fourth ventricle in all Selachians.

No plexus develops in the tela chorioidea telencephali medii in Ganoids, but in Acipenser, von Kupffer ('93) figures a plexus formation arising from the anterior wall of the velum trans


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versum, and Terry ('10) describes such a formation in Amia, as well as folds which appear on the caudal wall of the velum. The tela chorioidea diencephali itself forms a large thin-walled dome with no plexus formation. There is a plexus in the roof of the fourth ventricle. Lateral telencephalic choroid plexuses according to Burckhardt ('94) are absent, but Hill ('94) writing of Amia says: "It (the paraphysis) may be thought of as an isolated portion of the roof of the fore-brain which owes its existence to the formation of the folds marked Pl.chr. in figure 20, and which are themselves the representatives of the choroid plexuses of the lateral ventricles."

Of the Urodeles, Burckhardt ('91) has described extensive plexuses developing both from the tela chorioidea telencephali medii and from the tela chorioidea diencephali in Ichthyophis. Warren ('05) shows the enormous diencephalic plexus of Necturus absorbing also the entire caudal wall of the velum transversum. There is a plexus in the roof of the fourth ventricle. The lateral telencephalic plexuses are present and arise from the base of the median telencephalic plexus (plexus inferioris) as has been attested by Mrs. Gage ('93), Studnicka ('93), Warren ('05) and Burckhardt ('91). Burckhardt ('91) says of Ichthyophis: "Die Plexus der Hirnhemispharen aber spalten sich je in zwei Stamme von denen der eine sich gegen das Zwischenhirn ausstreckt, und in der Folge zuerst sich in Zweige spaltet, indess der andere in den Hemispharenventrikel eindringt und sich sodann in zwei Zweige spaltet, einen nach rtickwarts umbiegenden, welcher den Ventrikeltheil des Temporallappens und einen, welcher das iibrige Vorderhirn versorgt." And Warren ('05) writes concerning Necturus: "The telencephalic plexus develops from the paraphysal arch " "The plexuses of the hemispheres arise on either side from the origin of the telencephalic plexus and pass into the lateral ventricles."

Concerning the Chelonia, Humphrey ('94) shows a plexus arising from the tela chorioidea telencephali medii in Chelydra serpentina, as does also C. L. Herrick ('91) in Cistudo. Warren ('11) states that the plexus is not present in Chrysemys marginata and with this statement my observations agree. The "two



'MORPHOGENESIS OF THE CHOROID PLEXUSES 511

paired masses growing backward from the origin of the lateral plexus into the diencephalon" of which Warren writes do not seem to me to be at all homologous with the median telencephalic plexus. They arise too far posterior on the plexus; are at no time connected with the roof plate; and are merely prolongations of the lateral plexus. The diencephalic plexus is not so well developed as in Urodeles but is present in all forms, as is also the plexus of the fourth ventricle. Humphrey ('94) shows in Chelj'dra serpentina the lateral telencephalic plexus arising from the base of the median telencephalic plexus and passing into the lateral ventricle. According to Warren ('11), in Chrysemys marginata, "The plexus chorioideus laterahs springs from the paraphysal arch immediately in front and lateral to the mouth of the paraphysis, figure 25, and invaginates the dorso-mesial wall of the hemisphere."

In considering the Mammalia, considerable space will be given to interpreting accurately the velum and paraphysis. This is rendered necessary if one is profitably to homologize the lateral telencephalic plexus of Mammalia with the same structm-e in the lower vertebrates. Since, as we shall see later, the jiarai^h}'sis never appears in Mammalia excei)t as an arch of the roof plate of the telencephalon in early stages of development, it will be referred to as the paraphysal arch. ^Nlinot ('01) used the term 'to apply to the entire roof plate of the telencephalon between the velum transversum and the lamina terminalis, a sense in which it is no longer used.

The only observations of value dealing with the Monotrenies are those of Th. Ziehen ('05) on Echidna hystrix and G. Elliot Smith ('97) on Ornithorhynchus, and these leave much to be desired. Smith describes the origin of the lateral telencephalic plexuses and a structure which he says "constitutes the paraphysis of Selenka." I do not know what ex'idence he had for stating that the structure he describes is the paraphysis of Selenka for so far as I ha^'e been able to determine, Selenka has nowhere a description of the paraphysis but merely the bald statement that it is present in Marsupials. Smith's statement probably implied no more than that he interpreted this structure as the

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 26, NO. 5



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paraphysis. Extracts from this paper follow and will be discussed later.

The lamina suprancuroporica takes a sudden bend backwards (fig. 3) to form a horizontal band, which gives origin in many lowly vertebrates to the plexus inferioris, and in higher animals to the plexus lateralis as well, or exclusively. In the specimen under consideration, however, although the plexus laterales do not actually spring from this lamina, they are formed from the caudal prolongation of its lateral

parts In describing the structures met with in a medial

sagittal section it was mentioned that the dorsal part of the (actual) anterior wall of the median cavity of the forebrain was bulged out to form a large sac. The corresponding structure is well seen in the early

embryo of Parameles In the Platypus embryo, however

(fig. 2), a well developed choroidal fold extends from the superior commissure to the lamina from which the lateral plexus arises, completely invaginating the paraphysis (figs. 7, 9 and 15) in the middle line. In Platypus the transition from optic thalamus to paraphysis is a very gradual one, so that in examining a series of coronal sections the lateral walls of the diverticulum would seem to be merely the forward continuation of the ependymal layer of the Fliigelplatten (fig. 15).

As a matter of fact, the appearances in this series of coronal sections are not deceptive at all, the sac being undoubtedly just what it appears to be, an anterior pouch of the choroid plexus of the diencephalon, the lateral walls of the pouch being actually the forward continuation of the Fliigelp'atten. A glance at figures 1, 2 and 3 will make this quite apparent. The similarity would be much more obvious if figure 3 were from a coronal instead of a transverse section. In front of this pouch lies the velum transversum and then the roof plate of the telencephalon (lamina supraneuroporica as he calls it), from the caudal prolongations of the lateral parts of which arise the lateral telencephalic plexuses. In a later article, Smith ('03) reaffirms his belief that the anterior extremity of the lateral telencephalic plexus arises from the roof plate. The embryo is doubtless too far advanced to show the true paraphysal arch.

Ziehen's work on Echidna is eminently unsatisfactory from the standpoint of this discussion, because the sections he shows invariably skip the anterior end of the lateral telencephahc plexus. He has but one suggestive statement referring to this region:



MORPHOGENESIS OF THE CHOROID PLEXUSES



513



Im Bercich des Sulcus hemisphaericus ist die mediale Hemispharenwand verdiinnt und taschwartig in das Heniispharenlumen eingestiilpt. Diese Tasche entspricht dem Plexus chorioideus ventriculi lateralis. Sic offnet sich also in den Sulcus hemisphaericus (und zwar in seine laterale Wand) in der Decke des Foramen Monroi und conmiunieirt sowohl mit der Sichelspalte wie mit dem hinten obsteigenden zwischen Zwischenhirn und Heniisphareuhirn gelegenen Absclmitt des Sulcus hemisphaericus.




P'ig. 1 Coronal section from the forebrain of an oinhryo of Paramelea nasuta. Copied from Smith. Labels mine.

Fig. 2 Coronal section from the forebrain of a foetal Ornithorhynchus. Copied from Smith. Labels mine.

Fig. 3 Transverse section through the forel>rain of a 10 mm. human embryo. H 173, Chicago Eml)ryological Collection. Slide L'l, Section 11. X 13 J.

REFERENCE LETTERS



a.a.c.l.L, anterior area chorioidea tel encephali lateralis CO., chiasma opticum c.p., commissura posterior C.S., corpus striatum d-t.gr., di-telencephalic groove ep., epiphysis f.c, fissura chorioidea f.M.. foramen interventriculare hem., hemisphere wall hy., hypothalamus Li., lamina terminalis mes., mesencephalon n.a.L, nucleus anterior thalami n.o., nervus opticus p.a.c.t.l., posterior area chorioidea tel encephali lateralis



p.a., p.t.L, pars anterior i)le.\us telen cephali lateralis par., paraphysis p. p., p.t.L, pars posterior ple.xus telen cephali lateralis r.inf., recessus infundibuli r.m., recessus mamillaris r.posl., recessus postopticus r.pre., recessus preopticus Led., tela chorioidea diencephali t.c.t.in., tela chorioidea telencephali

medii i

l.f., taenia fornicis th., thalamus

t.r-p., telencephalic roof-plate t.L, taenia thalami v.L, velum transversum



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The 'Sichelspalte' I understand to be the cleft between the hemispheres in front of the diencephahc roof. The lateral telencephalic plexus, then, must extend anteriorly beyond the velum transversum into the roof plate of the telencephalon.

Ziehen also is inclined to interpret the anterior extremity of the diencephalic roof in Echidna as the paraphysis. He remarks:

Das ganze Bild erinnert an die Paraphyse mancher Reptilien. Ich stehe auch nicht an, diese leichte fordere Zuspitzung des hinteren Kuppelgebietes der Paraphyse homolog zu sitzen, wie im vergleichenden Abschnitt specieller erortert werden soil. Eine tiefere Einsenkung hinter der Zuspitzung — etwa im Sinne eines Velum transversum — f ehlt. Vor der Zuspitzung beginnt sofort die Einsenkung der Fossa interhemisphaerica.



ted





Fig. 4 Section from the forebrain of a 6| mm. embrj^o of Echidna hystrix. X 30. Copied from Ziehen. Labels mine.

Fig. 5 Transverse section from the forebrain of a 14 mm. pig. no. 18, Chicago Embryological Collection. Slide 5, section 19. X 25.

In an older embryo of which he says, "Sehr bemerkenswerth is wiederum das Verhalten des Kuppelgebietes des Zwischenhirns gegen die Fossa praediencephalica hin," he describes nothing resembling a velum transversum and a comparison of figures 4 and 5 will show the resemblance of his 'Kuppelgebietes' to the anterior pouch of the tela chorioidea diencephali of a pig embryo. If the plane of section in figure 5 were homologous with that of figure 4 the resemblance would be much more striking. If it be really the paraphysis, it forms a good transition stage to the condition found in higher Mammalia.



MORPHOGENESIS OF THE CHOROID PLEXUSES



515



Observations on the Marsupial brain are remarkably meagre. I have been able to find but two statements bearing on the subject. Broom ('97) says of a 14.8 mm. embryo of Trichosurus vulpecula: "The choroid folds into the lateral ventricles, is partlj^ formed, and the paraphysis well marked." He has no figures of sections. Selenka ('91) has a simple statement that the paraphysis is present in Marsupials, presumably in the opossmn. Bis jetzt habe ich die Paraphyse bei embrj'onen von Haifischen, Reptihen, und Beuteltieren beobachtet, zweifle jedoch nicht, dass sie alien Wirbeltieren gemeinsam ist." That is all, but I hope soon to fill this gap.




Fig. 6 Sagittal section of the forcbraiii of a 15 mm. pig. Copied from Johnston. X 10. Labels mine.

Fig. 7 Sagittal section of the forebrain of a 11 mm. embryo of Erinaceus europaeus. Copied from Gronbcrg. X 10. LabeLs mine.



Thanks mainly to Gronberg, the brain of the Insectivora is better known. His work was done with Erinaceus euro])aeus. Ziehen ('06) says of Tupaja, "Die Verhilltnisse gleichen den fiir den Igel beschriebenen in hohem Masse."

Gronberg's figures 25, 26, and 27 show clearly the velum transversum and paraphysal arch although he is loath to call them so. A comparison of figures 6 and 7 will make this plain. He describes also plexuses in the diencephalon and fourth ventricle. Of the lateral telencephahc plexus he writes:



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Die Adergeflechtsfurche entstcht am friihesten. Sie ist schon bei meinom Stadium C (11 mm.) vorhandcn und sowohl ausgebildet, dass ihre crsto Entstehung sicher aiif cinem Ijedeutend jungern Stadium zu suchen ist. Doch fiiidct sich auf Stadium B (8 mm.) noch keine Spur einer Faltenbildung. Die Form und das Aussehen der Falte ergeben sich aus den Figg. 52 und 53. Man sieht, dass sie in ihrem vordern Theil weiter in die Hemispharenhohle hineinreicht, als es mehr caudalwiirts der Fall ist. Es zeigt sich auch, wenn man eine Schnittserie durchmustert, dass die Falte nach hinten allmahhch kleiner wird und schlicsslich nur eine leichte Einbuchtung darstellt, welche nach hinten ganz allmahlich verstreicht. Der vordere Theil dagegen verhallt sich ganz anders. Die Falte ist hier tief und erstreckt sich mit ihrem freien Rand weiter nach vorn als die mit der iibrigen Hirnwand in Verbindung

stehende basis Auf den folgenden Stadien vergrossert sich

die Adergeflechtsfalte bedeutend, besonders in ihr vorderer, freier Theil, ....




Fig. 8 Cross section through the forebrain of a 15 mm. embryo of Erinaceus europaeus. Copied from Gronberg. X 10. Labels mine.

Fig. 9 Cross section through the forebrain of a 32 mm. human embryo. H41, Chicago Embryological Collection. X 25. Slide 29, Section 6.

One would conclude from this description that the anterior end of the lateral plexus had arisen the earlier, and that it arises from the roof plate of the telencephalon is clearly shown in his figure 54, which is here reproduced with a section from a human embryo for comparison (figs. 8 and 9). Again if the section of the human embryo were a coronal instead of a transverse section, the similarity would be more obvious.



MORPHOGEXESIS OF THE CHOROID PLEXUSES 517

Of the forms between Insectivora and Man nothing of value is known. Ziehen ('06) shows sections of the lateral telencephalic plexus of Tarsius spectrum, a prosimian, but not in the proper plane to be of value, and again describes the anterior pouch of the diencephalic roof as the paraphs-sis.

Sehr beachtenswert ist auch, dass unmittelbar hinter der Fossa praediencephalica die epitheliale Dccke des Z\\-ischenhirns sich zu einer stulen Falte, welche an die Parapliyse erinnert, erliebt und dass erst einige Schnitte weiter occipitahviirts diese steile Falte durch den nicdiane Plexus des 3. Ventrikels eingestiilpt wird.

In an earlier paper, the author (Bailey, '15) called attention to the true homologue of the paraphysis in the human embryo and insisted upon its position in the telencephahc roof plate just anterior to the velum transversum. Previously, Streeter ('12), Francotte ('94) and D'Erchia ('90) had written of the paraphysis in the human embryo. Streeter homologizes the anterior pouch of the diencephalic roof with the paraj^hysis, and from a comparison of Francotte 's figures witli sections of embryos of approximately the same stage, I am convinced that he mistook the same structure for the paraphysis. D'Erchia shows a section from a 30 mm. human embryo in which he labels a structure 'paraphysis' which seems to me to be merely an oblique section of the lateral telencephalic i)lexus.

In his model of a LS.O nmi. human embryo. His shows clearly the lateral telencephalic plexus coming off lateral to the paraphysal arch, but his statement ('04) of the origin takes no account of this fact. "Sein deni Thalanms angehefteter Randstreifen bleibt epend\^nal und in ihm bildet sich die Fissura chorioidea, von der aus die Epithelfaltungcn des Corpus chorioideum in den Seitenventrikel sich einstiilpen."

Hochstetter ('13) in his account of the development of the lateral telencephalic plexus in the human embryo shows one figure (fig. 6) of a section through the plexus which passes also through the telencephahc roof plate, but his description contains nothing concerning the origin of this part of the plexus.

D'Erchia ('96) considers the lateral telencephalic plexus to be derived from the \'elum transversum: Per questa parte volga



518 PERCIVAL BAILEY

tutto quello che si e detto per la cavia. Dal velum per diverticoli lateral! di formano i plessi emisferici inferiori destro e sinistro, dei qiiali uno e disegnato nella fig. 28."

Finally the author (Bailey, '15) has presented an account of the development of the lateral telencephalic plexus which it is the purpose of the present piper to supplemant.

Concerning these structures in other groups of vertebrates this discussion is not so much concerned, but a few words at least about the lateral plexus in other vertebrates will not be out of place. This plexus is not present in Teleosts (Burckhardt, '94) nor Anura (Herrick, '10). In Lacertilia its development has been described by Tandler and Kantor ('07) and Warren ('11) and agrees in all essential respects with that hereinafter detailed for Chrj^semys marginata. In examining some young alligators in the collection of Dr. Elizabeth Crosby, the posterior part of the lateral telencephalic plexus was found to be present, but very small and poorly developed. The brain of an adult pigeon was also examined and the lateral telencephalic plexus was seen arising from a plexus formation in the roof of the telencephalon, but of the posterior part of the plexus there was no sign except a plexus of blood vessels along a thin but uninvaginated medial hemisphere wall. Dr. C. Judson Herrick suggested that this may represent a stage in the phylogenetic development of the plexus. Mrs. Gage ('95) figures the brain of the embryo of the English sparrow. Both the figures and the context show that the' lateral telencephalic plexuses arise from the median telencephalic plexus and just lateral to the paraphysis, apparently not invaginating the medial hemisphere wall. She writes : In the young sparrow ( g. 2) the paraphysis occurs in the midst of a mass which gives off the paraplexuses, and it opens directly dorsad of the portas, i.e., into the aula. . . . It is noticeable in the older embryo that 1;he union of the auliplexus with the paraplexuses lies dorsad of the porta (fig. 14)." The works of Neumayer ('99) and Hochstetter ('98) contain nothing of value for the present discussion. The two invaginations which they describe are temporaTy and unimportant. A similar condition is shown in my figure 19 (Bailey, '15). D'Erchia ('96)



MORPHOGENESIS OF THE CHOROID PLEXUSES 519

considers the lateral plexus in the guinea pig to be derived from the velum transversum. "E dal velum che si origina il plesso del III ventricolo e i plessi coroidei emisferici destro e sinistro." It is interesting also to note that although Tilney ('15) correctly labels the paraphysal arch in models of the brains of young cat embryos, in later stages he invariably transfers the label to the anterior pouch of the diencephalic roof. Johnston ('09) has correctly interpreted the paraphysis in pig embryos, but his statement that the lateral telencephalic plexus appears as a folding of the anterior wall of the velum transversum is misleading for ho immediately follows with the statement that it is separated from the velum by tlic i^araphysal arch.

In the angle between the vesicle and the dicncepluilon appears the chorioid plexus pushing into the lateral ventricle. It appears as a folding of the anterior wall or limb^jf the velutn transversum and its lateral prolongation. In this way ai)pe:ir.s the chorioid fissure whose further history need not be traced. Near the median line the plexus apjiears as a fold projecting into tiic interventricular foramen and separated from the velum transversum by the paraphysal arch.

MATKI{IAL AND .MHTHODS

The material on which this study is based consists of a series of twelve embryos of Chrysemys marginata from mj'- own collection, ranging in size from 5.1 mm. greatest length to one having a carapace 10.0 mm. long, and an 8.8 mm. embryo from the Harvard Embryological Collection, very kindly loaned to me by the Harvard Laboratory. All of my material was fixed in Zenker; stained in bulk with borax carmine; embedded by the celloidin-paraffin method; cut at 10m in transverse series; and counterstained on the slide with orange G. The excellent preservation of the form relations of the delicate membranous portions of the brain may be attributed to the method of embedding. The embrj'os were all passed from 95 per cent alcohol to etheralcohol; then through 0.5, 1 and 2 per cent celloidin; hardened in chloroform alcohol, and cleared in benzol, before embedding in paraffin. The Harvard embryo is cut in 10 m sagittal sections and stained with borax carmine and eosin.



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The forebrains of four embryos — 1 a, greatest length 5.1 mm.; H. E. C. no. 1433, greatest length 8.8 mm. ; 5 b, carapace 8.6 mm.; and 4 b, carapace 10.6 mm. — were reconstructed by the Born method at a magnification of 100 diameters. Millimeter plates were used and every section drawn. It was necessary to dissect the models rather extensively to expose- the fissura chorioidea. The models were stacked from a side view of the head drawn from a photograph, with the exception of the Harvard embryo. This latter embryo was cut sagittally and the stacking was guided by the epiphysis and paraphysis. Since the embryo was not cut in an exactly sagittal plane, after the paraphysis and epiphysis had passed out of the plane of section, most of the lateral telencephalic plexus had been stacked and the remaining sections were added with no other guide except comparison with other models.

DESCRIPTION

This description will be confined to the lateral telencephalic plexus, since concerning the other plexuses I find no reason to differ from Warren's account, with the exception noted in the history.

The main landmarks of the region in which the lateral telencephalic plexus develops are already laid down in an embryo of 5.1 mm. greatest length. Figure 26 shows the roof plate of the forebrain in such an embryo and figure 10 shows the same region schematically represented. The roof plate of the telencephalon, back of the lamina terminalis, appears as a triangular area (only half of it shown in figure 26) its base formed by the velum transversum and its apex lying at the posterior end of the lamina terminalis while from its center arises the paraphysis. The lateral sides of the triangle are formed by the taeniae fornices. At the lateral angles of the triangle, taenia fornicis, velum transversum, taenia thalami and di-telencephalic groove meet. It is not possible accurately to determine this point in the embryo under consideration because the roof-plate has been but imperfectly differentiated histologically, but in later stages these angles of the triangle may be easily located.



MORPHOGENESIS OF THE CHOROID PLEXUSES



521



The earliest unquestionable appearance of the lateral telencephalic plexus is in the Harvard enibrj'o, 8.8 mm. in length. It appears here as a crescent-shaped ridge projecting into the lateral ventricle, with two more strongly developed points showing as small elevations (fig. 22). The anterior extremity of the plexus lies clearly in the roof of the telencephalon lateral to the paraphysis and medial to the taenia fornicia. The taenia fornicis appears in figure 22 as a ridge apparently in the medial hemisphere wall. It bears here a very close superficial resemblance to the hippocampal ridge in a young human embryo, but its later development and internal structure show plainly that




Fig. 10 Diagniiii of the region around the paraphysis in tlie roof of the forebrain of a 5.1 mm. emiiryo of Chrysemys marginata.

Fig. 11 Diagram of the same region in an embryo of 8.8 mm.

Fig. 12 Diagram of the same region in an embryo having a carapace of S.6 mm.



it is the taenia fornicis. Its apparent position in the medial hemisphere wall is an illusion produced by the invagination of the plexus between it and the paraphysis. The triangular area of the telencephalic roof plate is well marked and the lateral angles can be determined. A sagittal section through the triangle is practically a straight line, except for the evagination of the paraphysis (figs. 13 and 21) as are also parasagittal sections (fig. 14). Nevertheless the lateral angles are depressed and the sides of the triangle are concave outward. Transverse sections through this region are therefore curved and convex upward (fig. 21). The velum trans versum sharply dehmits the telencephalic roof plate at the base of the triangle (fig. 14).



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Figure 15 shows ;i parasagittal section still farther laterally through the triangle. The velum transversum is obvious, the plexus invaginating the roof plate medial to the taenia fornicis and tilting the portion of the roof between itself and the taenia. Above and lateral to the taenia fornicis the brain wall is histologically differentiated; medial it is ependymal. This difference is much more apparent in later stages (fig. 17). Posteriorly the plexus is less well developed and as we approach the lateral angles of the triangle, plexus, velum, and taenia fornicis tend to merge into one groove which becomes continuous with





Fig. 13 Sagittal section no. 135 from an 8.8 mm. embryo of Chrysemys marginata. Harvard Embryological Collection, no. 1433. X 33j. Fig. 14 Parasagittal section no. 130 from the same embryo. Fig. 15 Parasagittal section no. 124 from the same embryo.



the di-telencephalic groove. Lateral and anterior to the point where the taenia thalami meets the di-telencephalic groove and velum transversum the hemisphere wall is massive and uninvaginated. It would seem, then, that in this embryo, the lateral telencephahc plexus lies entirely in the roof plate of the telencephalon. The condition is diagrammatically represented in figure 11.

Figures 23 and 24 depict the region around the foramen of Monro in an embryo with a carapace 8.6 mm. long, about 14 mm. greatest length. Figure 23 looks at the foramen of the right half of the brain from the medial side. The cephalic end of the



MORPHOGENESIS OF THE CHOROID PLEXUSES



523



model is, consequently to the left. The paraphysis which had been removed is represented by a line of white dashes. Figure 24 looks at the same foramen from the lateral side. The model is therefore reversed and the cephalic end points to the right.

The condition of the roof-plate is diagrammatically represented in figure 12. The differentiation between hemisphere wall and




Fip;. IG Transverse section from the forebrain of an embryo of Chrysemys marginata having a carapace 8.6 mm. in length. Embryo 5 b, slide 13, sect. 11. X 33 J.

Fig. 17 Transverse section of the same embryo; section IG, slide 13. X 33J.

roof plate is clear and the taenia fornicis obvious (figs. 10 and 17). The anterior extremit}' of the lateral telencephalic plexus arises plainly from the telencephalic roof plate lateral to the paraphysis and medial to the taenia fornicis (fig. IG). Figure

17 shows a section posterior to figure 16 through the main body of the plexus, the plexus still b'ing in the roof plate. Figure

18 is of a section still farther posteriorly. The plexus is here shown crossing the taenia fornicis into the medial hemisphere wall. The taenia fornicis is now medial to the plexus and drop


524



PERCIVAL BAILEY



ping down to meet the anterior nucleus of the thalamus, which it does in a few sections and becomes continuous with the taenia thalami. In figure 19, much farther posteriorly, the taenia thalami is present, the plexus being entirely in the medial hemisphere wall. The portion of the plexus arising from the medial hemisphere wall is very poorly developed (fig. 19) but its area of invagination is extensive (fig. 24).

In later stages this posterior part of the plexus develops more rapidly and overshadows the other. Figure 25 shows a lateral




Fig. 18 Transverse section of the same embryo as figure 16. Slide 13, section 22. X 33 J.

Fig. 19 Transverse section of the same embryo; section 5, slide 14. X 33|.

view of the region around the foramen of Monro in an embryo with a carapace of 10.6 mm. A pen sketch of the entire model is appended (fig. 27) showing the region represen ed in figure 25. (Figure 24 is of a homologous region in a younger embryo.), The fissura chorioidea appears merely as a big hole in the medial hemisphere wall; all the landmarks are lost. In still later stages, this hole becomes reduced to a long narrow slit.

The development of the plexus in size and shape is so well discussed and figured by Warren ('11) that it will not be considered here.



MORPHOGENESIS OF THE CHOROID PLEXUSES 525

DISCUSSION

From the foregoing history and description, and from an analysis of the remaining hterature, for in the history are included only the most important papers and especially those deaUng with the lateral telencephahc plexuses, it will be seen that there are certain definite regions of the brain wall wherein choroid plexuses develop. These regions and the plexuses which develop from them may be tabulated as follows:

Tela chorioidea telencephali medii— Plexus telencephali medius Anterior area chorioidea lateralis telencephali — Plexus telencephali lateralis (below Chelonia)

{Anterior area chorioidea lateralis telencephali — Plexus tclencoi)hali lateralis (Chelonia and above) Posterior area chorioidea lateralis telencephali (heraispherici) — Plexus telencephali lateralis (Chelonia and above) Velum transversum — Plexus velares Tela chorioidea diencephali — Plexus dicncephali Tela chorioidea mcsencephali — Plexus mesenccphali Tela chorioidea myelenccphali — Plexus myclencephali

Tilney ('15) has suggested that the saccus vasculosus should be reckoned with the choroid plexuses in the forms where it is present and in this opinion I concur. It is best developed in those forms in which the diencephalic plexus is rudimentary or absent, i.e., in Cyclostomes, Selacliians and Ganoids. The plexus formation is ver}' poorly de\'cloi)ed in Urodeles and never again present. There should be added to the above therefore:

Rccessus infuiuiibularis (posterior wall) — Saccus vasculosus.

The myelencephalic ]ilexus arises in the roof of the fourth ventricle, tela chorioidea nwelencephali, in every known vertebrate above Amphioxus.

The mesencephalic plexus is found only in Petromyzon, where it arises from the mesencephalic roof, tela chorioidea mesencephah.

The diencephalic plexus arises from the tela chorioidea diencephali. Appearing first in Cyclostomes, but very poorly developed, it disappears almost entirely in Selachians, where the tela chorioidea diencephali is almost completely absorbed



526 PERCIVAL BAILEY

by. the overgrowth of the vekim transversum. In Ganoids, the tela chorioidea diencephaU begins to emerge, forming a thin walled sac, and in Urodeles is again invaginated by an enormous diencephalic plexus. It may be that the diencephalic plexus in Selachians and Ganoids is represented by the choroidal folds on the posterior limb of the velum, developing from the anterior portion of the tela chorioidea diencephali which has been drawn down into the velum transversum by the overgrowth of the latter. The diencephahc plexus is present in all forms above Urodeles but is never again so well developed.

The velar plexuses are present only in Selachians, Ganoids, and Urodeles. They may involve either the diencephalic limb or telencephalic limb, or the entire velum transversum. The choroidal folds on the diencephalic limb have been homologized, in Selachians and Ganoids, with the diencephalic plexus of other forms, and with some reason. The choroidal folds on the anterior limb are not homologous with either the median or lateral telencephalic plexuses.

The median telencephalic plexus arises from the tela chorioidia telencephali medii, just in front of the paraphysis (paraphysal arch of Mammalia), from the Selachians to the Chelonia, inclusive, with the apparent exception of the Ganoids. It is not constantly present in Chelonia and is never found in Mammalia. Its development seems to be in inverse ratio to the degree of development of the lateral telencephalic plexus and the latter in direct ratio to the size of the hemispheres.

The lateral telencephalic plexus is found in all groups of vertebrates from the lowest to the highest in the line of ascent of Mammals with the exception of the very lowest, Amphioxus and the Cyclostomes. Apparently sporadically and imperfectly developed in Selachians and Ganoids, it is present constantly thereafter. We have stated previously that it is absent in Teleosts and Anura, with which we are not concerned. In all forms below Chelonia, it develops in what I have called elsewhere (Bailey, '15) the anterior lateral telencephalic chorioidal area, in the roof plate of the telencephalon between the paraphysis and the taenia fornicis of the medial hemisphere wall. Where the median



MORPHOGENESIS OF THE CHOROID PLEXUSES ;V2<

telencephalic plexus is strongly developed the lateral plexus appears to be an appendage of it (Necturus, Warren); where the velum is involved in an extensi\'e plexus formation, the lateral plexus appears to be an appendage of it (Acanthias. Minot); but always arises from the region of the telencephalic roof plate described above, and medial to the taenia fornicis.

With the Chelonia comes a change. The lateral plexus arises in the anterior area chorioidea lateralis telencephali as has been previously described but in its later de\elopment crosses the taenia fornicis and invaginates also the i)osterior area chorioidea lateralis telencephali in the medial hemis]ihere wall. Such a condition is found also in the (Jecko brain (Tandler and Kantori. This imohement of the medial hemisphere wall comes more and more to i:)redominate in the development of the lateral plexus as the hemis])heres come more and more to dominate the devol(»))inent of the telencephalon, but even in the highest Mannnaha the anterior extremity of the lateral choroid ])!exus dev(^loi)s from the loof plate of the telence]ihnlon and th(^ evidence ni:iy briefly be summarized hci'e:

(a) Elliot Smith ('S)7) in describing the br.-'iii of a foelal Oi uiIhorhyncus described the lateral choroidal plexus as arising from the continuation backwards of the horizontal jxirt of the lamina sui)raneui'oporica, which term he used to include all the i-oof plate of the telencej^halon between the velum transversum and the lamina terminalis. Again in 190.'?. he reiteiated his belief that the anterior extiemity of the latei:il chomid;!! j)Iexu< :iii>c^ from the roof plate.

(6) Th. Ziehen's figures of l^chidii;', do not show l\w anterior extremity of the lateral plexus, but he states that it opens into the Sichelspalte. that is, into the cleft between the hemisi)heies anterior to the diencephalon, as well as the sulcus hemisphaerieus (di-telencephalic groove) .

(c) Observations on the ]\laisu]iials up to i)resent ie\eal nothing.

(d) Crronberg states of Erinaceus euro])aeus that the anterior extremity of the lateral plexus is better developed in his earliest stage than the posterior extremity and appai-ently arises fii-st.

THE JOURXAI. Ol- COMPARATIVE XEUROI.OGV, VOL. 26, NO. 5



528 PERCIVAL BAILEY

'J'his Iiokls true of all iiiMininals and is what one would expect from the phylogenetic history of the plexus. His figure 42 of a section anterior to the velum shows clearly the anterior extremity arising from tlie roof plate of the telencephalon.

(e) The earliest appearance of the plexus in the human embryo occurs in His' embryo of 13.6 mm. and his model shows clearly the plexus arising just lateral to the paraphysal arch.

(/) Hochstetter ('13) figures a section of a human embryo showing the anterior extremity of the plexus, and the author recently (Bailey, '15) has described three human embryos showing the plexus extending into the roof plate alongside the paraphysal arch anterior to the velum transversum.

(g) Collateral evidence is derived from the development of the lateral plexus in other mammals, for example, Johnston ('09) states that in the pig the plexus arises from the anterior limb of the di-telencephalic groove but is separated medially from the velum transversum by the paraphysal arch.

CONCLUSIONS

1. The lateral telencephalic plexus of Chrysemys marginata arises from the anterior area chorioidea lateralis telencephali in the roof plate of the telencephalon between the paraphysis and the taenia fornicis of the medial hemisphere wall and in its later development oversteps the taenia fornicis just anterior to the point where taenia fornicis, taenia thalami, velum transversum and di-telencephalic groove meet, and invaginates also the posterior area chorioidea lateralis telencephali in the medial hemisphere Wall, just anterior to the di-telencephalic groove. The pars anterior plexus telencephali lateralis which develops from the anterior area chorioidea lateralis telencephali in earlj^ stages is much larger and better developed than the pars posterior plexus telencephali lateralis, but in later stages develops much less rapidly than the pars posterior.

2. All the data at present available support the conclusion that the lateral telencephalic plexus arises from the anterior area chorioidea lateralis telencephali in the roof plate of the telencephalon between the paraphysis (or paraphj'-sal arch) and the



MORPHOGENESIS OF THE CHOROID PLEXUSES 529

taenia fornicis in all vertebrates where it is present, but that in Chelonia and the forms above, it oversteps the taenia fornicis and invaginates the posterior area chorioidea laterahs telencephaU in the medial hemisphere wall and that this latter portion comes more and more to dominate its development as we ascend the vertebrate scale.

I wish here to express my gratitude to Dr. S. Walter Ranson for his unvarying kindness and interest throughout the progress of this work.



Literature Cited

Ahlbohn, F. 1883 Untersuchunpicii iihcr das (Idiirti dci- I'cdoinyzDiitcii.

Zcits. wiss. Zool., Bd. 39. Haii.kv, p. 1915 The inorpholofj;y of the roof i)Iat(' of the forchraiii and the

lateral choroid i)lexuse.s in tho human ondjiyo. Jour. ('onip. X(!ur.,

vol. 2(;. Bl.\kk, J. A. 1000 Tlic roof aiui lateral recesses of I he fourth ventricle, considered int)i'i)liolojiically and enihryologically. Jour. Coinp. Neur.,

vol. 10. Bkoom, J. 1897 The embryology of Trichosurus vulpecula. Proc. Roy. Soc.

of N. S. Wales, vol. 27. BuRCKHARDT, R. 1891 Untcrsuchuiigen am Gehirn und (leruchsorgan von

Triton und Ichthyophis. Zeitschr. f. wiss. Zool., lid. 52.

1894 Der Bauplan des Wirbeltiergehirns. Morjjh. Arheiten von G. Schwalbe, 4.

D'Erchia, Fl. 1896 Contributo alio studio della volta del cervello intermedio e della regione parafisaria in embrioni di pe.sci e di Mammiferi. Monitore Zoologico, vol. 7, pp. 118 and 201.

Francotte, p. 1894 Note sur I'oeil parietal, I'cpiphyse, la ])araphyse et les plexus choroides du troisieme ventricule. Bull, de I'Acad. roy. de Belg., no. 1.

Gage, Mrs. S. P. 189 ; The brain of Diemyctylus viridescens. Wilder (QuarterCent. Book. ■ 1898.

1895 Comparative morphology of the brain of the soft-shelled turtle (Amyda mutica) and the English sparrow (Passer domesticus). Prf)c. Am. Micr. Soc, vol. 17.

Gronberg, Gosta. 1901 Die Ontogenese eines niedern Siuigergehirns nach

Untersuchungen an Erinaceus europaeus. Zoolog. Jahrb., Abth. Anat.,

Bd. 15, p. 261. Herrick, C. J. 1910 The morphology of the forebrain in Amphibia and Reptilia.

Jour. Comp. Neur., vol. 20. Herrick, C. L. 1891 and 1893 Topography and histology of the brain of certain

reptiles. Jour. Comp. Neur., vols. 1 and 3. Hill, C. 1894 The epiphysis in teleosts and Amia. Jour. Morph., vol. 9, p. 237. His, Wilhelm. 1904 Die Entwicklung des menschlichen Gehirns. Leipzig. HocHSTETTER, F. 1898 Beitrage zur Entwickelungsgeschichte des Gehirns.

Bibliotheca Medica., Abthg. A., Heft. 2.

1913 liber die Entwickelung der Plexus Chorioidei der Seitenkammern

des menschlichen Gehirns. Anat. Anz., Bd. 45, pp. 225-238. Humphrey, O. D. 1894 On the brain of the snapj>ing turtle. Jour. Comp.

Neur., vol. 4. Johnston, J. B. 1909 On the morphology of the forebrain vesicle in vertebrates.

Jour. Comp. Neur., vol. 19. Kappers and Carpenter 1911 Das Gehirn von Chimaera monstrosa. Folia

Neuro-Biologica, Bd. 5. Kingsbury, B. F. 1897 The encephalic evaginations in Ganoids. Jour. Comp.

Neur., vol. 7.


KuPFFKU, C. VOX 1S93 Die Entwickliing des Kopfes von Acipenser sturio.

Studien zur vergloichendcn Entwicklungsgoschichte des Kopfes der

Kranioten. Heft. I., Miinchen.

1903 Die Morphogenio des Xervensystems. Oskar Hortwig's Hand buch. MiNOT, C. S. 1901 On the morphology of the pineal region based upon its

development in Acanthias. Am. Jour. Anat., vol. 1. Xeumayer, L. 1899 Studien zur Entwicklung-sgeschichte des Gehirns der

Ssugetiere. Fcstschr. z. 70 Geburt.stag von C. von Kupffer. Jena.

Fischer. Selenka, E. 1891 Das Stirnorgan der Wirb.'iticre. Biol. Centralbl.. Bd. 10. Smith, G. Elliot 1897 The brain of a foetal oniithorhynchus. Quart. Jour.

Micros. Sci., n. s., vol. 39.

1903 On the morphology of the cerebral commi.ssures. Trans, of

the Linnaean Soc, London., vol. S. part 12. Stekzi, CJ. 1907 II sistema nervoso centrale doi vertebrate. Vol. 1, Ciclostomi. Stueetek, G. L. 1912 The development of the central nervous system. Keibel

and Mall's Human Embryology. Studnicka, F. K. 1S93 Zur Lisung einigcr Fragen aiis der .Morphologic des

\'orderhirns der C'ranioten. .\nat. .\nz.. Bd. 7. Tandlkh, J. A\u KanToh, H. 1907 Beitnige zur Entwickelung des Vertebrat engehirns. I. Die Enfwickelungsgeschichtc des Geckohirnos. .Vnat.

Heflc. Bd. 33. Heft 101. Teiuiy, H. .1. I'.tlO 'i'lic inorpliology of the pineal region in teleosts. Jour.

.M..rpl... vol. L'l. TiL.N'EV, FuEDEUKK 191.^ The morphology of the diencejihalic floor. Jour.

Conip. Xeur.. vol. 2o, no. 3, pp. 213-2S2. Wahhe.n, John- 190") The development of the paraphysis and pineal region in

Xecturus maculatus. .\m. Jour. .Vnat., vol. o, |)p. 1-29.

1911 The development of the paraphysis and |)ineal region in reptilia.

Am. Jour. Anat.. vol. 11, pp. 313-392. Ziehen, Tii. 1904 \'erhand. Kon. .\k. van Wetensch. te .Vmsterdam. 26 Nov.

(pp. 331-340).

1905 Zur Entwickclungsgeschichte des Centralnervensystems von

Echidna hystrix. Jenaischc Denkschriften, Bd. VI, 2. Theil.

190G Morphogcnie des Centralnervensystems der Sjugetiere. Oskar

Hertwig's Tlaiidbuch.



PLATE 1

EXPLANATION OF FIGUKES

The reference letters for all figures are found on page 513. It is impossible to portray all the topography of the region around the foramen interventriculare by means of drawings. For aid in orientation, the position of the principal landmarks is indicated on the models as follows: the taenia fornicis by a line of dashes; the velum transversum by a line of crosses; the taenia thalami by dots; and the di-telencephalic groove by dots and dashes alternating. The cross sections will also aid. On figures 22 and 23 the positions of the sections are indicated by arrows. Since the models are tilted, the arrows indicate accurately only the points where the sections cross the lateral telencephalic plexus.

20 Median view of the fore brain of a 5.1 mm. embryo of Chrysemys marginata. Embryo 1 a. X 50.




PLATE 2

EXPLANATION OF FIGlIRKh



21 Median view of the forebrain of an S.8 mm. embryo of Chrysemys marginata. Embryo 1433. H.E.C. X 40.

22 Lateral view of the forebrain of an 8.8 mm. embryo of Chrysemys marginata. Embryo 1433. H.E.C. X 40. Lateral hemispheio wall I'omoved.





EXPLANATION OF FIGURES

23 Median view of the region around the foramen interventriculare in an embryo of Chrysemys marginata having a carapace 8.6 mm. in length. Embryo 5 b. X 100. In order to show the fissura chorioidea it was necessary to remove the paraphysis and represent the fissure slightly higher than it really is.



EXPLANATION OF FIGURES

24 Lateral view of the same region as in figure 23. Lateral wall of the hemisphere and plexus telencephali lateralis removed, exposing the fissura chorioidea. Embryo 5 b. X 100.



PLATE 5

EXPLANATION OF FIGURES

25 Lateral view of the region around the foramen interventriculare in an embryo of Chrysemys marginata having a carapace 10.6 mm. in length. Embryo 4 b. X 66|. Lateral hemisphere wall and lateral telencephalic plexus removed, exposing the fissura chorioidea.

26 Dorsal view of the forebrain of a 5.1 mm. embryo of Chrysemys marginata. Embryo 1 a. X 80.

27 Pen sketch of model of entire forebrain of embryo 4 b, showing the area from which figure 25 was taken. X 25.