the carotid labyrinth in hyla aurea, with a note on that in leiopelma hochstetteri

24 Pages·2005·4.7 MB·English

[ 503 ]
THE CAROTID LABYRINTH IN HYLA AUREA, WITH
A NOTE ON THAT IN LEIOPELMA HOCHSTETTERI
BY J. B. CARMAN
Anatomy Department, University ofOtago, Dunedin, New Zealand
INTRODUCTION
The presence of a specialized structure at the bifurcation of the common carotid
artery in the Amphibia has been known for well over 100 years. This structure,
which has been variously called the carotid gland, the carotid labyrinth, or the
carotid body, is a well-marked swelling, partly cavernous and partly plexiform, at
the termination of each common carotid artery; from it arise the external carotid
(orlingual) andtheinternalcarotidarteries. Thelabyrinthoccursinallthecommon
species of urodeles and anurans, but is said to be absent in the Gymnophiona-
limbless, burrowing Amphibia.
Since first described byHuschke in 1831, it has beengiven manyfunctions, such
asthatofanaccessoryheart(Hyrtl,1838; Sabatier, 1873; Boas, 1882, 1883);agland
(Stannius, 1846); and(aviewstillprevalent)ameansofensuringforthecarotids the
most richly oxygenated blood (Brucke, 1852; Zimmermann, 1887). Others, com-
paring it with the carotid body of Amniotes, see in it a possible chemo-receptor:
de Boissezon (1939), forinstance, says it contains cells very like those in the mam-
malian carotid body, and recently Chowdhary (1951) has made a similar claim;
Pischinger (1934), however, denies this, believing that it contains only ordinary
vascular elements. Then again, because Meyer (1927) found depressor fibres in the
glossopharyngeal nerve and since this sends a branch to the organ, some have
assumed it to be a pressor-receptor: thus, Ask-Upmark (1935) likens it to the
mammalian carotid sinus (and perhaps to the extracranial rete mirabile in some
lemuroids), and Neil, Strom & Zotterman (1950) also incline to the same opinion,
although, apart from one solitary instance (Palme, 1934), sensory endings have, to
my knowledge, never been found here. De Boissezon (1939) regards the labyrinth,
not asaspecialpressoreceptor, but rather as a mechanical regulatorofthe cerebral
blood pressure; and Pischinger (1934) has suggested that it actively controls the
volume of blood entering the internal carotid, a control necessitated, he believed,
by the amphibious habits ofthe animal.
The internal anatomy of the organ has been studied in detail by relatively few
workers (Zimmermann, 1887; Pischinger, 1934; Eloff, 1935; and Ishida, 1954); of
these only Ishida has given adequate illustrations of its interior, while the only
reconstructionisthatbyPischinger, andeventhisshowsonlyapart. Histologically,
some speak of it as muscular, others as fibro-elastic, while de Boissezon calls the
tissueoftheplexusa'plasmodium'. Eloff(1935) hasdescribed initcellsresembling
nerve-cell bodies.
In contrast to the somewhat incomplete and controversial accounts ofits struc-
ture and functions, the development of the labyrinth has been more thoroughly
investigated and, apart from an initial error by Maurer (1888), the results, on the
504 J. B. Carman
whole, agree. Marshall(1893),forinstance, describedtheprocessinRanatemporaria
asfollows: inthetadpolethebronchialcirculationistypicallythatofagill-breather-
in each arch an afferent vessel from the truncus lies immediately caudal to the
efferent vessel, going to the dorsal aorta, the two being joined at first only by the
gill-capillaries (Text-fig. 1A); later (12 mm. stage) they become connected more
directly, ventral to the capillary loops, by a small channel (Text-fig. 1B), which so
do
ec
A comm.
ch.
B
- to I
C
Text-fig. 1. Schematic drawings illustrating the development of the external carotid and the
vascularchangesinthefirstandsecondbronchialarchesatmetamorphosis(afterMarshalland
Pischinger). A, 9mm. stage; B, 12mm. stage, just before metamorphosis; C, just after
metamorphosis. Gill capillary loops are represented by broken arrows, andthe direction of
blood flowisshown bycontinuous arrows. Formeaningofabbreviations intext-figures and
Plate see p. 525.
enlarges at metamorphosis that blood from the heart can now pass directly to the
dorsal aorta through the efferent vessel, thegills receivingless andlessbloodas the
pulmonary circulation is established (Text-fig. 1C). Each external carotid anlage
arises (9 mm. stage) in the floorofthe mouth as a short blind lumen (Text-fig. LA)
whoseposteriorendsoonturnsoutwardsanddorsallytowardstheventralendofthe
efferent vessel ofthefirst arch, which itjoins (12 mm. stage), the two thenforming
one continuous vessel. Itis nearthisjunctionthatthecommunicationbetweenthe
afferent and efferent vessels occurs (Text-fig. 1B). This communication, at first
Amphibian carotid labyrinth 505
small and single, later becomes plexiform with three or four openings into each
vessel, andfromthisplexus, says Marshall, thedefinitivecarotidlabyrinthdevelops.
In Rana, the communication between the afferent and efferent vessels results
from canalization of a plate of cells between them, not only in the first arch but
alsointhe others. Maurer (1888) originally thoughtthesecellscomefromthebran-
chial epithelium, andbesides entering into theformation ofthelabyrinth also form
accessoryepithelialbodiesbetweenthegreatvessels; accordingtoPischinger(1934),
however, the cell-plates in Rana are not bronchial in origin, but come from the
endothelium ofthe two vessels-cells from the bronchial epithelium, he says, take
nopartwhateverintheformationofthecarotidlabyrinth. Mishima'sresults(1944)
in the anurans Rhacophorus arborea and Bufoformosus substantially confirm these
findings. InB. vulgaris, however, Pischingerfound no cell-plates, and said thatthe
communications ariseherebyasimplebreaking-throughoftheapposedvesselwalls.
Because there is no satisfactory account ofthe carotid labyrinth in English, and
becauseofthecommonmisconceptionsanduncertaintiesregardingitsstructureand
function, I have undertaken a detailed study ofits gross anatomyand histological
structure, and a brief study of its innervation, in a local species of anuran-Hyla
aurea-aswell as reviewingall the available relevant literature. Also Ihavebriefly
studiedtheorgan in thenativefrog,Leiopelmahochstetteri. Ithasnotbeenpossible
here to include a study ofthe development ofthe organ in either species.
MATERIAL AND METHODS
The investigations were mainly on Hyla aurea, of which I had a plentiful supply
from the Physiology Department ofthis University, to whom my thanks are due.
The animals were killed by pithing, pinned in the supine position, and dissected,
underabinocularmicroscope, to showthe carotidlabyrinthandrelatedstructures;
the precise relations were confirmed by making a graphic reconstruction of the
post-hyoid region and thefloorofthemouthfromaspecial series stained withiron-
haematoxylin and picrofuchsin.
Labyrinths were fixed in Zenker's orBouin's fluid, embedded in paraffin, serially
sectionedat 10/sandstainedwithhaematoxylin-eosin, azo-carmineandanilineblue,
iron-haematoxylinandpicrofuchsin, andwithresorcin-fuchsinforelasticfibres. The
post-hyoid regionandbuccalfloorofoneanimalwasfixedinBodian'ssolutionno. 4
(formol-formic), serially sectioned in paraffin at 10/s, and stained by Bodian's
activated-protargol method.
Threewax-platereconstructions (150x)ofonelabyrinthweremade,takingevery
section in a 10/s H.-E. series. One (A) was ofthe walls ofthe organ; a second (B)
was acastofthe interiorofthe common carotid artery, the mainchamber, and the
external carotid; while the third (C) was a cast of the tributaries of the internal
carotid.
Withpermission ofthe MinisterofInternalAffairs, Iwas able to studythelaby-
rinth in the rare native frog, Leioplema hochstetteri, which is rigorously protected.
I dissected four of these animals, and one labyrinth was serially sectioned at 10/,
and stained with iron-haematoxylin and picrofuchsin. I am greatly indebted to
Mr S. G. Gittos ofWarkworth, Auckland, for collecting these specimens for me.
33 Anat. 89
506 J. B. Carman
RESULTS
I. Hyla aurea
The carotid labyrinth is exposed as follows:
Stage I. The skin is incised along the mid-line, and across the pectoral region
between the fore-limbs. The four flaps are then reflected, after cutting the two
lymph-sac septa connecting the skin to the underlying muscles: anteriorly, the
septum submaxillaris; more posteriorly, the septum pectoralis (Text-fig. 2). The
anterior flaps are dissected back to the mandible and removed; the posterior flaps
ima~~~~~
1~~~~~
1 cm
Text-fig. 2. The superficial muscles exposed by stage I ofthe dissection.
(Text-figures 2-4were drawn from photographs.)
are reflected laterally and trimmed off to expose the entire pectoral region. This
discloses the following muscles (Text-fig. 2): m. intermandibularis anterior, in the
tip ofthe jaw; m. interinandibularis posterior, a muscular sheet between the man-
dibles; and on each side, m. deltoideus; m. sternoradialis; m. pectoralis, in two
parts (pars sternalis and pars abdominalis); and finally the segmented m. rectus
abdominis.
Amphibian carotid labyrinth 507
Stage II. The approach to the axillary region, where the labyrinth lies, now
involves removal of the clavicle, coracoid and associated muscles. First of all,
m. intermandibularis posterior is detached from the mandibles and removed, thus
exposing the omosternum. Then a blade ofthe scissors is inserted between the two
parts ofpectoralis, about halfa centimetre from the mid-line, and passed forwards
beneath the pars sternalis and the underlying bones, being kept hard against the
bones to prevent damage to underlying structures. The bones and muscles are
Text-fig. 3. Thedeeper muscles exposedby stage II ofthe dissection.
cleanly cut through, on both sides. Holding the omosternum, the whole centre-
piece of the pectoral girdle is carefully dissected from the underlying sternohyoid
muscles. The fore-limbs are pulled firmly apart and re-pinned, and so the axillary
spaces are clearly exposed. The following muscles are now in view on each side
(Text-fig. 3): hyoglossus muscle, alongside the mid-line; just lateral to and parallel
with it, is geniohyoid arising caudally by two slips embracing the insertion of
sternohyoid; sternohyoid, more caudally, also arises by two slips, from the dorsal
surface of the xiphisternum and the rectus abdominis; and lastly, the slender
omohyoid, which runs anteriorly, medially and ventrally to a common insertion
33-2
508 J. B. Carman
with sternohyoid into the hyoid bone. Between omohyoid and sternohyoid thereis
atriangularintervalwithitsapexanteriorly: thisisthefocalpointofthedissection,
for in here lies the carotid labyrinth.
StageIII. Sternohyoid isnowcutthroughcaudallyand, workingfromitsmedial
border to protect the underlying structures, it is reflected rostrally and cut away
cleanly between the slips of geniohyoid. The axillary space is thus fully exposed
as in Text-fig. 4. Laterally, is the root of the fore-limb; medially, the pharynx
andlarynx; anteriorly, theposteriorwallofthebuccal cavity (extendingouttothe
angleofthejaw); andposteriorly, m. obliquus abdominis separatingthespacefrom
the pleuro-peritoneal cavity.
mcv
cct
Text-fig. 4. Theleftaxillaryregionexposed bystage IIIofthe dissection. Anteriorisabove, and
medialto theleft. Theleftsternohyoid muscle (sh)has beencutawayandtheleftomohyoid
(oh) has been cutandretracted laterally. The anteriorpart ofthe externaljugularvein (ejv)
has been cut away.This animal was anomalous in that the hypoglossal nerve (hn) passed
forwards deep to the omohyoid; otherwise the course is quiite typical.
In the mid-line, the bulbus arteriosus emerges from the pericardium and divides
at onceinto two branches, the rightandleft truncusarteriosus. Eachrunsrostrally
and laterally and soon divides into three main arteries. The most posterior is the
pulmo-cutaneous artery, arching first dorsally and then caudally. Anterior to this
is the aorta, which arches dorsally and somewhat rostrally (it finally turns medially
and caudally). Just lateral to the point where these two arteries first diverge there
is a prominent gland-like structure-the jugular body-which, as an outstanding
feature of the axilla, is a very useful landmark, although, in certain species, it
Amphibian carotid labyrinth 509
should be noted, it is more anterior and may even be rostral to and medial to the
carotid labyrinth (Romeis, 1926). Finally, the most anteriorbranch ofthe truncus
is the common carotid artery, which is slightly narrowerthan theothers and runs
anteriorly, aswellasdorsallyandlaterally, thusgraduallydivergingfromtheaorta;
it ends, after a course of 1-2 mm., in a more or less well-marked swelling-the
carotid labyrinth (Text-fig. 5).
Thecarotidlabyrinthis about 1 mm. longandischaracterizedbyitsdarkpigmen-
tation. From it spring two arteries: the internal carotid, which, as the apparent
continuation of the common carotid, continues to arch dorsally; and the smaller
PC
ta
Text-fig. 5. The greatvessels ofthe leftside, seen fromtheventral aspect.
(Drawn froma camera lucida sketch.)
external carotid, which leaves the rostral aspect of the labyrinth close to the ter-
minationofthecommoncarotid,and, afterpassingalittlemedially,runsanteriorly
under omohyoid into the floor of the mouth (Text-fig. 4). The hypoglossal nerve,
emerging laterally from under omohyoid, sweeps medially and ventrally over the
aorta, then rostrally over the carotid labyrinth, finally dividinginto two branches;
these continue rostrally, ventral to the insertion of omohyoid, and then over the
external carotid to lie medial to it. The glossopharyngeal nerve at first follows
a similar course to the hypoglossal, although a little more anteriorly and laterally.
Itcrosses theoriginoftheinternal carotidtoenterthefloorofthemouth, lateralto
the external carotid and beneath omohyoid. The laryngeal branch of the vagus
nerve lies more deeply and, passing caudally and medially, winds round the lateral
aspect ofthe pulmo-cutaneous trunk.
The veins ofthe axilla (Text-fig. 4) are delicate and thin-walled. They comprise:
thesubclavian vein,commencinglaterallyattheunionofthebrachialandmusculo-
cutaneous veins and sweeping medially overthe caudal wall ofthe space;the inno-
minate vein, comingfrom the junction ofthe subscapularwith theinternal jugular
tojointhesubclavianvein; andtheexternaljugular, whichbeginsinthefloorofthe
mouthandrunsdirectlycaudally, ventraltothecarotidlabyrinthandtheIXthand
XIIthnerves, andlateraltothejugularbody-itfinallyjoinsthesubclavianveinto
form the superiorvena cava, which opens into the sinus venosusundercoverofthe
projecting pericardium.
510 J. B. Carman
The epithelial bodies, or parathyroid glands (Text-fig. 4), two on each side,lie
just medial to the external carotid artery a little in front of the carotid labyrinth.
A prominent fat-body is often present between the origins of the hyoglossus
muscles and is possibly a seasonal phenomenon (Text-figs. 3, 4).
Ventral
- cch.
L ant.lot.
ram. [ec]
vmidd. /at.
ram.[ec]
o o
V') ._
a0-
m ot. prox.
llat. dis.
trunk
car.
Dorsal
Text-fig.6. Thelateralhalfofarightcarotidlabyrinthlookingfromthemedialaspect.Thelateral
portionofthecapillaryplexus (cap.plexus) andthelateraltributaries ofthe internal carotid
areshown.Theorganisdividedintoitstwoparts,parscavernosaproximallyandparscapil-
laris distally, at the arbitrary plane indicated by the arrows. (Text-figures 6-11 are from
tracings, made onadioptograph, ofthewax-plate reconstructions B and C.)
The carotid labyrinth
Morphology
Superficially, the carotid labyrinth in Hyla is adistinct swelling 1 mm. longand
06 mm. across, rightatthebifurcationofthecommoncarotidartery, whichreaches
it at its proximal pole.* The smaller external carotid leaves the labyrinth just
anterior to the common carotid and passes medially and anteriorly, the two vessels
* Theterms ofreference usedindescribingthecarotidlabyrintharenotalwaysconsistentand
aresometimesconfusing, sothatdifficultiesareencounteredwhencomparingtheworksofdifferent
authors. Zimmermann, for instance, has described the organ as if seen from the ventral aspect
whereasIhaveregardeditasaportionofthearterialarchIII,whichpassesfromventraltodorsal.
Thusthe proximalpole, which I describe as ventral, he calledmedial, andthe distal pole, which
Iconsiderasdorsal,hedescribedaslateral. Consequently,thesurfaceswhichhecallsventraland
dorsal, I have calledlateral andmedial.
Amphibian carotid labyrinth 511
forming an angle with each other of 900 or even less (Text-fig. 5). Leaving the
opposite (distal) pole ofthe labyrinth is the internal carotid artery.
Although superficially the external and internal carotids appear to arise from the
opposite poles of the labyrinth in a perfectly simple and straightforward manner,
their actual origins internally are, in fact, very complex; for the common carotid
artery does not lead directly into either vessel: shortly afterentering the swelling it
dilates, somewhat asymmetrically, into alarge chamber (the main chamber) which
discharges on the one hand into the external carotid by six separate channels, and
on the other into the internal carotid through a mass ofcapillaries and a system of
collecting vessels (Text-fig. 6).
The common carotid artery, when it reaches the labyrinth, has a bore of about
0*25 mm.; it runs into theorganforabout 0*2mm. before actually openingintothe
main chamber; this opening is slightly oblique so that the posterior wall of the
common carotid is longer than the anterior (Text-figs. 6, 7).
The main chamber is 0*5 mm. long and about 0 4 mm. across.Proximally, is the
opening into it of the common carotid posteriorly, while more anteriorly are the
openingsoutofitoftheexternalcarotid. Distally,areahostofsmallorificesleading
toacapillaryplexus. Infact,theentirelabyrinthmaybesaidtopresenttwoparts-
proximal and distal. The proximal part ('pars cavernosa' of Zimmermann) com-
prisestheterminationofthecommoncarotid, theoriginoftheexternalcarotid, and
the associated part of the main chamber. The distal part ('pars capillaris' of
Zimmermann) contains the capillary plexus and the associated portion ofthe main
chamber, as well as the various tributaries of the internal carotid which drain the
capillary plexus (Text-fig. 6; PI. 1, fig. 1).
The external carotid artery arisesfrom the main chamberby threeorificesoneach
side-posterior, middle and anterior. The anterior openings are the most ventral
while the posterior ones, which flank the opening of the common carotid into the
chamber, lie most dorsally (Text-fig. 6). Each opening leads centrally, that is
recurrently, into a corresponding ramw=. Ofthese, the posterior on each side is the
longest; itarchesventrallytojointhemiddleramus, whicharisesfromthechamber
just anterior and ventral to it. The common trunk so formed is then joined by the
smaller anterior ramus to form the lateral or medial root ofthe external carotid as
the case may be (Text-fig. 8). The lateral root now arches overthe proximal end of
the mainchamber, anteriortothecommoncarotid, anduniteswiththeshorterand
morevertical medialroottoform the externalcarotidartery(Text-fig.8). Thisthen
leaves the organ running medially and ventrally. In addition, the two roots may
communicatebyasmallaccessorychannelinfrontofthecommoncarotid(Text-fig.7).
Near their origins, the rami give off a number of small vessels which pass to the
capillary plexus (Text-figs. 6, 8). Furthermore, it is likely that they may present
minor variations; here, for instance, the lateral anterior ramus arose by union of
two smaller trunks, while each posterior ramus had a small collateral channel of
varying length each of which also sent a branch dorsally to the capillary plexus
(Text-figs. 7, 8).
The diameters of these vessels are approximately as follows: the rami, 0-08-
0'1 mm.; the roots, 0-12 mm.; the external carotid itself, 0-14mm. The accessory
communicating channel and the collateral channels were only 30-40Qt wide.
512 J. B. Carman
Thecapillaryplexusisatruerete mirabile, betweenthemainchamberonthe one
hand andthe internal carotid arteryontheother. Itforms, asitwere, acap fitting
over the distal halfofthe main chamber. It is thickest (0-2 mm.) at its centre and
tapers peripherally. Its concave, afferent aspect faces towards the main chamber,
and its convex, efferent aspect is related to the tributaries of the internal carotid
(Text-fig. 6).
Text-fig.7. Thecommon carotidartery(cc),mainchamber(mch.) andexternalcarotidartery(ec),
Postero-medial aspectseenfrom alittle dorsally. In Text-fig. 7-11, dorsalisbelow.
Ahostofafferent vessels ofsmallbore (20-40,#) leave the distal partofthe main
chamberandradiateoutintotheplexus. Theysoonbegintodivideandanastomose
freely witheachother, oftenformingloops, fromwhichsecondarybranchesproceed
(Text-fig. 8). As the result ofcontinued division and anastomosis a dense capillary
meshwork is formed, the smallest channels ofwhich are about 10/s wide and only
20-0/, long. Towards the convexity of the plexus the capillaries progressively
reunite into larger efferent vessels (20--30/) which finally drain into the various
tributaries ofthe internal carotid.
The internal carotid artery is fed by a system oftributaries which converge on it
overtheconvexsurfaceofthecapillarymass, fromitsrim; theyreceivetheefferent
vessels ofthe plexus and eventually form four main trunks, two proximal and two