THE MIDDLE EAR AND COLUMELLA OP BlftDS. 11

The Middle Ear and Columella of Birds.

Byfleoili-ey Smith, B.A.,

New College, Oxford.

IT may seem a supererogatory task to add to the pile ofliterature-which deals with the ear-bone homologies a straight-forward account of those anatomical and embryological factswhich may he ascertained by the examination of such familiartypes as the fowl and pigeon; but after a painstaking researchinto the literature of the Sauropsidau middle ear I haveunwillingly concluded that such a course was desirable.Although this literature is voluminous there is no singledescription of any Suuropsidan type which from a modernstandpoint cau be considered at all complete; that is to say,there is no account which describes in any one type—

1. The development and transformation of the auditoryossicles from the earl iest procar t i lage stage up-wards ;

2. The relations of the seventh nerve and chorda tyrnpanito the ossicles at different stages of development.

The words in italics are emphasised because a large partof the work on this subject fails to be conclusive owing to thelack oE sufficiently early stages of development, and this mostunfortunately is the case in the recent descriptions ofSphenodon by Howes (14) and Schauinsland (12). Kingsley(13) gives one isolated procartilage stage in a Lacertilian;

1 2 QEftbUTREY SMITH.

which serves to provej at auy rate, that tliese early stages areabsolutely necessary for the interpretation of the later.

The following essay will be divided into three parts :— (1)anatomical, in which certain new details are described, andan adequate account of the disposition of the chorda tympaniis given for the first time; (2) embryological, in which specialattention is paid to the derivation and homology of the stapesor proximal portion of the colutnella (an homology whichconstitutes the crux of the Sauropsidan middle ear); andfinally (3) a summary with some general conclusions.

I am much indebted to Mr. Jenkinson, Lecturer in Em-bryology in the University Museum, for his advice and agreat deal of material.

] . ANATOMY.

The Columel la (Fig. 1}—Anatomically the columella ofbirds is composed of two pieces, an inner ossified piece, thestapes, apposed to the fenestra ovalis, and an outer cartila-ginous piece, the exfcra-columella, united to the stapes proxi-nially, and attached distally to the tympanic membrane.There is no real joint between the stapes and extra-columella,bat great flexibility exists between the two, owing to thepliability of the cartilaginous neck which unites-them. Theextra-columella may be described as consisting of threepieces, supra-, extra-, and infra-stapedial, all perfectlycontinuous. The disposition of these parts is shown infig. 1, which represents the left columella of Gallus3 viewedfrom within the tympanum.

The columella is supplied with a single muscle, the tensortympani, which is attached to the infra-stapedial, andto the edge of the tyinpanic membrane, between the infi-a-and extra-stapedial cartilages. The muscle passes out of theear by a large foramen close to the stylo-mastoid foramen,curls round on to the back of the skull, and is broadlyattached to the basi-occipital bone in a shallow groove whichslopes nearly to the occipital condyle.

THE MIDDLE EAR AND COLTJMELLA 01" B1EDS. 13

The extra-oolumella is supplied with one ligament in allbirds, Platner's ligament, which stretches across the cavityof the middle ear to the posterior face of the quadrate bone{Pit., Figs. 1 and 8). In Gallus there are present twoother ligaments attached to the extra- and infra-stapedialswhich are in part concentrations of the fibrous constibnentsof the tympanic membrane ; I can only find these erroneouslydescribed by Parker (3) as being attached to the quadrate.In reality they pass beneath the quadrate, are continuedbeyond the region of the tympanic membrane into the liningof the Eustachian tube, and are finally attached to the wallsof tlie bony Eustachian groove near the point where itdebouches into the mouth (Fig. 2). This is a peculiar dis-position, not found in other birds that I have examined.

The Seven th Nerve.—This nerve has three branches,which are, counting in order from the root of the nerveoutwards, the sphenopalatine, the chorda tympani, and themain branch of the seventh. In Gallus the sphenopalatineand the chorda tympani come off together from the geniculateganglion and do not take up any intimate relation to the middleear. The chorda tympani, after its origin from the seventhnerve, runs a little way with it in the Fallopian tube, thenenters a bony canal of its own and so gains the posterior faceof the quadrate. The cross in Eig. '8 shows the approximatepoint at which the chorda tympani comes off the seventh nervein the fowl. After giving off the chorda the main branch ofthe seventh crosses the stapes externally and dorsally to it inthe cancellated bone, and then leaves the skull by the stylo-mastoid foramen.

In other birds, e. g. Columba, the chorda has a quitedifferent disposition (Fig. 3). It leaves the seventh nerve bya special foramen in the Fallopian tube just before the seventhnerve makes its exit from the sknll by the stylo-mastoidforamen; it then traverses a small piece of cancellated boneand enters the cavity of the middle ear quite superficially,viz. between the extra-columellaand the tympanic membrane.It now crosses the extra-columella, keeping this same relation

FIG. 1.—Left cohimella of Gsllus from inside tympanic cavity, pit.Platncr's ligament, exl. Extra-stapedial. exl. lig. Extra-stapedial ligament.inf. Infra.stapedial. inf. lig. Infra-stapcdial ligament, sttp. Supra-slapedial.slap. Stapes, muse. Tensor tjmpani.

tymp

F I G . 2.—Riglit ear of Gallus. External eai- is cut away, and the quadrateand bony roof of the lower tympanic recess are removed, fyiup. Tympanum.exl. External ear lining, extra coll. Extra-coliimcllav. ext. lig. Extra-stape-<iial ligament, inf. lig. Infra-stapedial ligament, muse. Teusor tymnani.car. Carotid, cat: can. Bony carotid canal, vn . Seventh nerve, east. BonyEastachian groove, eust. op. Opening of groove into nioutli.

THE MIDDLE EAR AND COLOHRLLA Of BIRDS. 15

to the tympanic membrane, namely lying just internal to itand external to the extra-columella, save that at the pointwhere it crosses the neck which unites the supra- and extra-stapedials it pierces the cartilage superficially.

t/nv

uctra^tap

FIG. 3.—Right ear of Columbn, Upper half of tympanic membranedeflected to show the structures upon its other side, slap. Stapes, suprastop. Supra-stapcdial. extra stap. Exlrfl-stapedial, pit. Platner's ligament.VII. Seventh nerve, ek. Chorda lympani. x Point at which chorda tympanicomes off in Gallus. tgm. Tympanum, qu. Quadrate. For this drawing Iam muck indebted to Mr. Darbisliire.

Having traversed the extra-columella, the chorda joinsPlatner's ligament and crosses the tympanic cavity in com-pany with it, so gaining the posterior face of the quadrate.This course of the chorda tympani has been, confirmed bymeans of serial sections in a late embryo of the starling.

The essential difference between the relations of the chorda

16 GEOFFREY SMITH.

bympaui in Gallus and in Columba may be seen in the follow-ing diagram.

I. Columella of Columba; II, of Gallas, from without, fp. Foot plu».slap. Stapes. Pit. Platner's ligament, vn. Seventh neive. ok. Chordatympani. supra, extra, and infra. Stapedial cartilages.

In these two relations of the chorda tympani bo the columella.we see a striking convergence towards the two conditions inLacertilia described by Versluys (10). In Lacertilta thechorda tympani may come off the seventh nerve behind thecolumella, and then run forwards, across, and external ordorsal to the extra-columella, or else it may come off: anteriorlyto the columella altogether (e. g. Gecko and those formswhich have no processes interims to the extra-columella).There can be little doubt that the backward origin is primi-tive, since Sphenodon shows it, and that the forward originin the fowl is secondary, as first suggested by Hasse {%), whosupposed that its forward, origin had to do with the peculiardevelopment of the quadrate articulation in that bird.

2. EMBRYOLOGY.

The middle ear cavity is formed from the first gill slit (5).The earliest stage which is instructive for the purpose inhand is the five-day-old chick. As yet no chondrifieation hastaken place, but the hyoid arch and the auditory capsule arerecognisably shown by the thicker aggregation of counective-

THB MIDDLE EAR AND COLUMELLA OF BIRDS. 17

tissue corpuscles in those regions (Fig. 4). The proliferationof tissue to form the hyoid tiroli takes placo from belowupwards; this is shown in the figures whore the more ventralportion of the arch Qiy.) is thicker than the more dorsal(stap.), the two portions passing into one another more or

I?IG. 4—Longitudinal (slightly horizontal) section through lijoid regionof five-day cluck.

less suddenly at the constriction, marked cons., fig, 4. Theseventh nerve crosses the hyoid arch just dorsal to the con-striction. The hyoid and auditory capsule proliferations arecompletely separate, being divided by a space where theconnective-tissue corpuscles are much more, thinly scatteredIt is seen in fig, 4 that the dorsal or proximal portion of the

18 GJBOPFBKY SAILTH.

liyoid ($tap.) lias approached quite near to the auditorycapsule, while tho latter shows no sign of sending an out-growtli to meet it.

PIG. 5.—Longitudinal section through six-day chick.

In the six-day-chiok the top of the hyoid has fused with,the auditory capsule, both being still in the pro-cartilaginouscondition. This is shown in Pigs. 5 and 6. Fig. 5 shows theseventh nerve crossing the hyoid above the constriction in

THE MIDDLE EAR AND OOMJMELLA OF BIRDS. 19

sensibly the same positiou as in the five-day-chick. It isquite clear from Figures 4 and 5 that no considerable out-growth from the auditory capsule can have taken place tocomplete the continuity of hyoid and auditory capsule. Thereis no evidence of such an outgrowth, and even if it occursbetween the stages Figs. 4 and 5, the outgrowth can only

FIG. 6.—Ditto; a more median section to sliow continuity of stapes withauditory capsule.

Letters used in Figs. 4, 5, and 6:i, E. Internal ear. Aim. CATS. Auditory capsule, STAP. Stapes, coys.

Constriction in hyoid arcli. UY. Hyoid arcli. CM. Cavity of middle ear.JUG. VEIN. Jugular vein, vn gn. Genieulate ganglion, vn. Seventh nerve.

Figs. 4, 5, and 6 drawn with camera under Zeiss 4, AA.

occupy a very small part of the space subsequently occupiedby the stapes, unless we imagine ib bodily thrusting thehyoid arch before it, a process which is not easy to imaginein ill-defined pro-cartilaginous stractm-eSj and for which thereis not the least shadow of evidence.

During the sixth and seventh days of incubation chondrifi-cation sets in. In the seven-day chick auditory capsule andliyoid are both perfectly chondrified and perfectly coutinnous

20 GEOFFREY SMITH.

%vith one another, the constriction observable in the five-and six-day chicks having, moreover, disappeared.

In the eight-day chick the stapes is divided off from theauditory capsole, and the extra-columella is severed from theextreme distal end of the byoid arch. This extreme end ofthe hyoid arch, which takes no part in the formation of theextra-colunaella is excessively small, only running througha few sections. My series of sections at this stage show thecontiuntty and homogeneity of the stapes and all parts of thecolurnella, the ossification of the stapes not occurring until alater period.

-I II III IVI. Jive-day cliick. II. Six-day. III. Seven-day. IV. Eight-day. All

viewed from without, and. caps. Auditory capsule, vu. Seventh nerve.ch. Chorda tympaui. cons. Constriction, br. Branchial blastema, extraroll. .Extra collumella. hy. Hyoid.

It should be plain from this account that the chondrifiedstages in the seven- aud eight-day chicks, with the descrip-tion of which previous authors have been content, really tellus little by themselves; but the previous history of the hyoidarch in the pro-cartilage condition shows (1) that the wholeof the extra-columella and part, at least, of the stapes areformed from i t ; (2) that the derivation of the foot-plug ofthe stapes, and perhaps the extreme distal part of thestapedial rod may be either from hyoid or from auditorycapsule, but from which of the two it is impossible to assert,since the two elements are already inextricably fused beforechondrification occurs; without leaving any visible boundarybetween them. It would be safe to say that certain cells in

THE MIDDLK EAK, AND COLUMELLA OF BIUDS. 21

the foot-plug are derived from the hyoid arch and certaincells from the auditory capsule. The important fact, how-ever, clearly expressed in Figs. 4 and 5 is that the dorsal partof the hyoid arch, i. e. the part lying between the seveuth nerveand the auditory capsule (sta/p. in ]?igs. 4, 5, and 6), givesrise to part, at least, of the stapes. The meaning of theconstriction in the five- And six-day chicks must remaindoubtful \ it corresponds in position to a division betweenhyomandibular aud keratohyal, and to the later divisionbetween stapes and extra-columella.

The following diagrammatic reconstructions will make theforegoing observations clear.

3. CONCLUSION.

The value of the embryological evidence here presented ispartly positive, partly negative.

Positively, it may be stated that in the chick the contribu-tion of the auditory capsule to the columella is exceedinglysmall, probably confined to the foot-plug of the stapes; atany rate the main part of the stapes and the whole of thecolumella is formed from the hyoid arch. Negatively, itproves the futility of basing arguments upon this question onisolated stages, or on cartilaginous stages which have notbeen traced back to their earliest procartiiaginous forerunners.Taking this into consideration the supposed derivation of thestapes of Sauropsida from the auditory capsule (9), and thepossible interpretation of Splienodon in this manner (12 and14) becomes exceeding doubtful; in birds, at any rate, as wehave seen, the condition confirms the opiuiou arrived at ontheoretical grounds by Gaupp (11), that the stapes of Saurop-sida corresponds to the stapes of Mammalia, and to the hyo-mandibular of fishes. Mammalia and Sauropsida have thismuch in common, that they have both converted the hyomandi-bular or dorsal portion of the hyoid arch into the stapes jbut subsequently they have gone on. different lines in evolu-tion, the Sauropsida making use of the more ventral part of

22 GEOFFllEY SMITH.

the hyoid to complete their chain of ossicles (extra-colnmella),while the Mammalia have pressed into this service the con-stituents of the arch in front—namely, the quadrate andarticular (incus and malleus).

(Since this article was in type "Versluys (15) has publisheda most thorough account of the development of the Lacertiliancolumella. I am happy to see that his results are in completeaccord with my own).

LllEBATUBE.

1. PiukT2tE.il, Jf.—' Bemerkungen iitaer das Quadrat-bein und die Pauken-holile der Vogel,' 1839.

2. HASSE, C.—"Zur Morphologic dea Labyrinths der Vogel," 'Anatom.Studien,' Bd. i, 1873.

3. PAHKER, W. K.—"On the Structure and Development of the Skull ofthe Common Fowl," 'Phil. Trans. Roy. SOB. Lond.,' vol. olix, pt. ii, 1869.

4. HtixLET, T. H.—"On the Representatives of the Malleus and Incus ofthe Mammalia in the other Vertebrate," ' Proc. Zool. Soc. Lond.,' 1869.

5. MOLDENHATJEE, W.—"Die Entwicklung des mittlerenunddcaaussereaOhres," 'Morph. Jahrb.,' Bd. iii, 1877.

fl. IIAGMIEN, L.—"Rechercb.es sue I'anatomie eomparee de la corde duI.ympan des oiseaux," 'Comptes Rendus de L'Academie des Sciences,' t. ci,1SS5.

7. GADOW, H.—'Phil. Trans.,' 1888, vol. olxxix.8. GADOW und SELENXA.—"Vogel," 'Bronn's Klassen und Ordnungen,'

Bd. vi, Abt. 4, 1891.9. HOFFMANN, C. K.—"Reptilien,"'Bronn's Klassen und Ordnungen,'

Bd. vi, Abt. 3, 1S01.10. VEUSLOTS.—"Die mittlere und aursere Obrsphiire der Laccartilia und

ltliyncoccplialia," 'Zool. Jahrb.,' Bd. xii, Heft. 2.11. GAurp, E.—" Oatogenese und Phylogensse des sehalleiteuden Appa-

rates bet den Wirbelthieren," ' Aniit. Hefte,' 2te Abt., 189S.(See this paper for discussion of whole question and complete list of

literal ute.)12. SCHATJINSLAND, H.—"Wdtere Beifcriige zui- EntwickluugsgcsohicliU

der Hatleria," ' Arch. Mikr. Anat.,' Ivi, 1900.13. KINGSLEY.—"The Ossioula Auditus of Vertebrates," 'Tuf.i's College

Reijoi-ts,' 1900.14. HQWJSS, 6. B., and S-WMMEMOK-, H. H.—" Developement of the

Skelelon of the Tualara," 'Trans. Zool. Soc. Loud.,1 vol. xvi, pt. i, 1901..15. VEBSbim, J.—"Eatwioklung der Columella auris bei den Laoer-

tilien," 'Zool. Jahrb.,' Bd. xix, Heft 1.