On the Cardiac Nerves of Some Cetacea, with Special
Reference to Those of Berardius Bairdii Stejneger

BY
TEIZO OGAWA(Received June 10, 1952)

The innervation of the mammalian hearts has very often become
the subject of profound and extensive studies in the anatomy as wellas in the physiology, and among a great many anatomists, who havedevoted themselves to this problem, especially His jr. (1891), Schumacher (1902), Perman (1924), and Worobiew (1928) are noted for theirvery fruitful researches. The detailed works of the last mentioned
author and his collaborators, Anujriew, Belowa, Schurawlew, Wolhynski,
etc., seemed to have left nothing important in the gross anatomy of
the cardiac nerves. Later, Nonidez (1939) made still a remarkableprogress, as he reported the possibility of discerning stain-technicallybetween sympathetic and parasympathetic fibers in the dog's heart,and quite recently Nomura by his microscopical works (1951, 1952) on
the cardiac nerves of the mouse contributed much upon the problem.
Nomura as well as Glomset (1940) insisted upon the abundance of nerve
fibers in or near the so-called conduction system of His jr. and Tawara.
The aim of the present paper lies mainly in mentioning my own
observations on the cardiac nerves in a fetus of the Pacific beaked whale,
Berardius bairdii Stejneger, for they contain some very different points
from the remarks of previous investigators, and though the materials
here treated are yet scanty, the results have, I guess, a greater meaning
than they at first look. Afterwards the cardiac nerves in two othersorts of the Cetacea, Balaenoptera borealis Lesson and Prodelphinus
caeruleoalbus Meyen, will be described, comparing with Berardius, as
the cardiac innervation of the Cetacea has attracted till today seemingly
very few attention of the anatomists.
Material and Method

The cetologically very interesting species, Berardius bairdii Stejneger(Japanese name: Tuchi-kujira), haunts our sea near Awa, the southern
province of Chiba Prefecture from June to September, mostly in summer.
The adult whales attain usually the body length of 10 m. Two fisherycompanies are erected to perform works for catch and utilization of

2

T. OGAWA

this beaked whale. The research materials were given us from thesecompanies.
The Sei whale (Japanese name: lwashi-kujira) treated in this paper
was caught near the Bonin Islands, and so it may belong to the Bryde's
whale, Balaenoptera brydei, rather than to Balaenoptera borealis (H.
Omura et al, 1952). But as this problem of identification is not yet
fully settled, the more common nomination will be adopted here.
The dolphin, Prodelphinus caeruleoalbus Meyen (Japanese name:Suji-iruka), is very abundantly seen and caught at Izu Peninsula inwinter (Ogawa, 1937). The villages Kawana and Arari are famous forthe dolphin fishery, and we got the materials there.
In the present work nearly always feta! hearts of them were dissected with naked eye and without any staining. Only sometimes theadult hearts were examined and a few microscopical preparations stainedwith hematoxylin-eosin or by van Gieson's method or by the Bielschowsky's method were also employed.
The fetal hearts are very appropriate for the observation of thenerves, for these are relatively well developed, and clearly visible
owing to scantiness of the adipose tissue and poor existence of theconnective tissue. Besides, the size is fitted for our treatment, theadult hearts of Balaenoptera and Berardius being too bulky to handle
for studying.
Observations

Berardius bairdii Stejneger (Figs. 1, 2, and 3)
One fetal heart, which is ea. 13,5 cm long measured straight frombasis to apex cordis, and ea. 14,0 cm wide in the transverse direction
at the height of the coronary sulcus, was examined. The heart had
been taken out by another person from a fetus of Berardius, the bodylength of which was about 1.8 m, and consulting the size it must
be in the later period of pregnancy.
Nearly the whole heart is undamaged, showing only a little wound
limited to the base of the left pulmonary vein. The cut out material
includes, besides the heart itself, the aortic arch, the Botallo's duct,
the pulmonary artery with its right and left rami, the lower portionof the trachea with bilateral bronchi, a portion of oesophagus withvagi attached to its wall, and some parts of thymus remaining near
the heart. The stem of the pulmonary artery is ea. 3,5 cm wide, while
the ascending aorta is ea. 5,5 cm in its greatest transverse diameter.

Cardiac Nerves of Some Cetacea, etc.

3

The left vagus, which is a large trunk of ea. 5 mm thickness,while descending on the ventral surface of the aortic arch, dispatchesat the height a little above the upper end of the Botallo's duct a
remarkable branch (A) mediocaudally (figs. 1 and 2). This branch
seems to consist mostly of vagal fibers, but partly to contain sympathetic
ones, as the vagus trunk shows anastomosis with the left sympathetic
near the origin of this branch and in addition the branch (A) itself
receives a few twigs from the left sympathetic.
The further course and distribution of A are noteworthy, for it

Fig. 1. Cardiac nerves of Berardius bairdii (anterior view)Dark·· -Right vagosympathetic

4

T. OGAWAruns down and to the right side always attached to the ventral surfaceof the ascending aorta, until it reaches above the beginning part of
the right coronary artery. On the way it shows two small connections
with sympathetic twigs coming from B, which will be related later.
The branch (A) is distributed, after dividing into many small rami, tothe upper lateral portion of the ventral wall of the right ventricle.
Anastomosis occurs very few between this branch and the nerves
existing on the ventral surface of the right atrium (fig. 1, *5). It is
important, that this A, departing from the left vagus and receiving
twigs from the left sympathetic nerve, undergoes during its wholecourse no large connection with the right nerves, definitely innervatesa certain part of the right ventricle.
Next the stout sympathetic branches (B and C) will be described(figs. 1 and 2). Both start, at first being united in a common trunk,
downwards from the middle cervical ganglion of the left side. This
trunk bifurcates at the height of the upper margin of the aorta into
two thick branches, anterior (C) and posterior (B).
The branch (B) descends behind the aorta in contact with the left
ventrolateral surface of the trachea and reaches the right side of the
Botallo's duct, after passing in front of the right pulmonary artery.
Behind the aorta it is divided temporarily into two portions, both ofwhich unite together again. Then it ramifies into two branches, right(B2) and left (B1).
B1 crosses over the later to be mentioned C1 , where very few fibers
seem to be exchanged between B1 and C1 at the crossing, and thenproceeds forwards and to the right side on the right upper surface ofthe pulmonary artery. Precisely persuing the rami and ramuli of BH
we know that this nerve reaches solely the conus arteriosus of theright ventricle, running there subepicardially in downward direction.
On the way it receives a small twig (*l) apparently coming from theright nerves. But as the right nerves show just at the origin of thistwig two small anastomoses (*2, *3) with the left sympathetic nerve(B2 ), it is not decided, whether the twig in question conveys fibers
originating from the right or from the left nerve.
B2 sends off at first a small ramus, which crosses over C1 dextral
to BH where no exchange of fibers is found between them, and thengoes down and forwards on the right upper surface of the pulmonary
artery. It then courses forwards under B1 and disappears as fine ramuli
from sight at the basis of the pulmonary artery.
The stem of Bz is strongly bent to the right side, and afterCardiac Nerves or Some Cetacea, ete.

5dispatching a branch forwards to unite with Cu shows two small anastomoses with D1 coming from the right side. These two anastomoses(*2, *3) are worthy of special attention, for in this fetal heart directcommunication between the nerves of both sides reaching in front of
the transverse sinus of the pericardium occurs only at these places, at
any rate in a very small amount. The stem of B2 goes then to theleft caudal direction and makes with C1 a large trunk (B2+C1 ), which

Fig. 2. Plexus cardiacus superficia1is of Berardius bairdii
Dark ... Right vagosympathetic

courses behind the pulmonary artery obliquely from right upper to left
lower and reaches the uppermost portion of the interventricular groove.
During its course posterior to the pulmonary artery no direct connection
exists between this trunk (B 2 + C1) and the later to be mentioned D2 +D3.
Branches of the trunk (B2 + C1) are followed to the medial part of theventral wall of the right ventricle adjacent to the interventriculargroove, in other words, to a part of the conus arteriosus, running in

T. OGAWA

apical direction from the left upper region (fig. 1).
The other thick branch (C) descends anterior to the aortic archand ramifies into three (CH C2, C3). One of them (C2), comparatively
the smallest, goes into the stem of the left vagus at a level between
the origin of A and the recurrens (fig. 1, R). Another branch (C3),larger than C2, ·turns to sinistral and reaches together with other left
sympathetic nerves and with a branch from the left vagus, after descending anterior to the left pulmonary artery, the wall of the left
atrium to continue into F, which will be related afterwards.
The thickest branch (C1) makes the stem of C, attains the rightside of the Botallo's duct and then the right upper surface of thepulmonary artery. Here it is crossed over at first by B1, later by abranch of Bz, while it courses to the right lower direction. Then it isfused with the stem and a branch of B2 , building so a large trunk(B2+C1), the course and destination of which were mentioned already.
In short, the conus arteriosus of the right ventricle is innervatedmostly, if not all, by rostrally originating sympathetic fibers of theleft side. These fibers descend partly in front of, partly behind theaorta and reach the destination passing dextral, and partially sinistral
to the basal portion of the pulmonary artery.
On the other hand, we see directly behind the aorta three nerves(D1, D2, D3) of various sizes, all coming from the right side, at first almost
parallel to each other, in an oblique direction on the right ventrolateralsurface of the trachea (figs. 1 and 2· ·-dark drawn). Though owing
to incompleteness of the material, their origins from the vagus andfrom the sympathetic trunk are not definitely determined, the largest
and middle placed D2 contains quite certainly both vagal and sympathetic
fibers, while the much smaller D1 and D3 consist nearly exclusively of
sympathetic fibers.
D1 lies a little upper than D2 and shows at the level of the lower
margin of the aortic arch two small anastomoses, proximal (*2) anddistal (*3), with B2 , as these were already mentioned in relation to B2.
At. the distal anastomosis D1 unites with D2 and just from the placeof this fusion a thin nerve extends down and forwards, on the way
receiving a small branch from D2 , and runs through the narrow space
between the aorta and the pulmonary artery to reach further a branchof B1. This thin nerve (*1) was accounted for already in the descriptionof B1. It _,. \ the only nerve, which apparently belongs to the rightnerves (D1> D2), and is distributed further together with the left nerves(B1)· But it is difficult at present to decide, whether its fibers originallyCardiac Nerves of Some Cetacea, etc.

belong to the right or to the left nerves, when one considers the small
anastomoses between B2 and Dr.
Dz is a stout, cylindrical nerve trunk and unites with the slightly
lower running Da in front of the right pulmonary artery. The large
trunk (D2 +Da), to which Dr also might be mixed (D2 +Da+Dr ?), proceeds
behind the pulmonary artery obliquely downwards and to the left sideand reaches above the left coronary artery, where it is divided into
three. It is quite remarkable, as pointed out above, that behind thepulmonary artery no direct connection takes place between D2 + Da andB2 +Cr.
Branches of D2 + Da, after repeated ramifications, go partly into theinterventricular groove, partly proceed into the medial part of the left
coronary sulcus, and innervate the ventral wall of the left ventricle.
One can see many of them run subepicardially either from the interventricular groove or from the medial portion of the coronary sulcus,
generally to the left caudal direction. They never follow the branchingsof the coronary artery, as the independency between nerves and vessels
is easily proven also in all other parts of the heart.
With enthusiasm I looked for anastomosis between D2 + Da and B2 + Cr
in this region, but found only a small one at the upper end of theinterventricular groove (*4). Besides, a twig deviates from the main
trunk of D2 + Da( +Dr?) to attain the lower part of the ventral surfaceof the left atrium, but it sinks for the most part into the depth ofthe coronary sulcus to be delivered with other branches of D2 + D3 tothe lateral marginal part of the left ventricle. Only a tiny anastomosis
was seen between this portion and the nerves on the ventral surfaceof the left atrium (*6).
Observing as the next step the heart from behind (fig. 3), theright and left relations of the cardiac nerves are quite unlike to thoseof the anterior view. Along the superior vena cava there are two
middle sized nerves coming from the right side and consisting probably
for the most part of the sympathetic fibers (D4 and D5). One of them(D 4) descends behind this vein and after ramification partly unites with
D5 , partly attain the terminal sulcus. The sinus node, if this be existent,
must receive this branch, though I could not ascertain the presence ofthe sinus node in Berardius.
D5 descends along the left side of the superior vena cava, and someof its branches reach the ventral surface of the right atrium, making
here plexus with a portion of branches arisen from D6 • This plexus
sends twigs to the right auricula and to the terminal sulcus. The

T. OGAWA

sinus node may receive these twigs too.
On the dorsocranial surface of the right atrium, more sinistral thanthe orifice of the superior vena cava a remarkable nerve plexus (*7)
exists directly ventrocaudally to the right pulmonary artery. It is
made chiefly by branches of D5 and D6 • One finds just in its neighbourhood a concentration area of the atrial musculature, corresponding
probably to the septal raphe reported by Papez (1920). D6 comes out
The·right uppermost

Ramus bronchalisFig. 3.

Cardiac nerves of Berardius bairdii (posterior view)
Rpa· ··Right pulmonary artery
Rpv· ·-Right pulmonary vein

more caudally than D2 from the right vagus as three separated nerves,
goes down partly to the ventral surface of the right atrium, partly tothe plexus on the dorsocranial surface of the right atrium (*7).
Two other branches (D7 ·and D8) start also from the right vagus
nearly at the same level as D6 , but more medially than this. D7 shows

Cardiac Nerves of Some Cetacea, etc.

9at the origin an anastomosis with the sympathetic nerve. D 1 and D8
descend posterior to the right pulmonary artery, except a small portionof D7' which goes to the ventral surface of the atrium. They makebehind this artery a remarkable nerve plexus (*8), to which besides
them the left vagus and the left sympathetic send also branches veryclearly. For the problem of the cardiac innervation this part surrounding the right pulmonary artery from before and behind, where thevagal and the sympathetic fibers coming from both sides meet together,seems to be the most important. The concentration area of the atrial
musculature lies just beneath the plexus in question. One branch fromthe left sympathetic can be traced a long distance (*9) from the dorsal
surface of the aorta to this plexus. Another branch belonging to
the left vagus (E1) is issued from E, which will be mentioned below.
Within this plexus (*8) the nerve bundles look here and there ganglionated, and the plexus sends to the hinder and lower direction a welldeveloped septa! nerve (S), which descends through the interatrial
septum to the fossula nervina of Worobiew.
D9 is a branch from the right vagus, issued more caudally than D8 •It descends at first behind the uppermost ramus bronchalis and reaches
further down the lower part of the remarkable nerve plexus, but it
continues more distinctly to the septa! nerve, apparently making its
main constituent. Fibers of the septa! nerve are distributed partly tothe dorsal walls of the ventricles, but partly disappear from sight,
sinking deeply at the left side of the orifice of the coronary sinus. In
the heart of an adult Berardius I could prove the intimate connectionof this deeply going nerve with the atrioventricular node of Tawara.
The septal nerve shows also anastomosis with F, viz. branches fromthe left vagus and left sympathetic.
The left vagus sends off a. fairly large branch (E) at the heighta little below the recurrens. After it runs to the right lower direction
for a short distance, it bifurcates, and the one branch (E1) turning
sharply to the right side enters the large plexus behind the right
pulmonary artery, while the other (E2) courses for a long distance on
the surface of the left atrium, and descends to the fossula nervina alittle sinistral to the septa! nerve, nearly parallel to this. It anastomoses on the way with a small nerve (D10) started very distally fromthe right vagus. At the fossula nervina the nerve (E2 + D10) lies more
superficially and more sinistral than the septa! nerve, but further
distribution of its fibers seems to be the same as that of the septa!
nerve.

10

T. OGAWAOn the dorsal surface of the left atrium a large assembly of nerve
bundles (F) run obliquely along the Marshall's vein. About one halfof them comes down from the left stellate ganglion and from thesecond and third thoracic ganglia of the left side (fig. 1), while about
the other half makes the continuation of C3 and of a branch (H) of
the left vagus, dispatched from this at the same level as E. All of
the sympathetic and vagal nerves descend in front of the aorta, thenof the left pulmonary artery, and reach the angle between the left
auricula and the left pulmonary vein. Here they are contained in theplica nervina of Worobiew, and then proceed to the coronary sinus, on
the way they give off small branches to the dorsal wall of the left
atrium. From the coronary sinus branches of F after making anastomoses
with the septal nerve and with E 2 + D10 are delivered widely over thedorsal surfaces of the right and left ventricles. Some fibers seem toattain the Tawara's node through the anastomosis with the septal nerve.
Nerves on the ventral surface of the left atrium show also an intimate
relation with the proximal part of F. Besides, a small nerve can betraced downwards from the sympathetic between the stellate and thesecond thoracic ganglia at first behind the aorta, then just before theleft pulmonary artery to the ventral surface of the left atrium (fig. 1,
not signed in the picture).
To summarize, the cardiac branches both of the vagus and thesympathetic going in front of the transverse sinus to the ventral wallsof both ventricles are crossed, at least for the greatest part. They
constitute the so-called superficial cardiac plexus, but in this plexus ofBerardius anastomosis occurs in a very small amount between the nervesof both sides. On the other hand, the branches distributed to bothatria and to the dorsal walls of the ventricles passing posterior to thetransverse sinus, do not cross, or at least the crossing is never clearly
seen. These belong to the so-called deep cardiac plexus, and in thisplexus anastomosis takes place very frequently between the nerves coming from both sides. Moreover it is worthy of notice, that the conus
arteriosus of the right ventricle receives chiefly sympathetic fibers
coming from the left side.
In addition one can definitely say that the nerves going to theventral walls of the ventricles depart from the stems of vagus andsympathetic at levels generally higher than those innervating the atria
and the dorsal walls of the ventricles. The nervous supplies to thesinus node of Keith and Flack and to the atrioventricular node of
Tawara will be discussed afterwards.

Cardiac Nerves of Some Cetacea, etc.

11

Balaenoptera borealis Lesson (Figs. 4 and 5)
The heart was taken out from a 120 cm long f etus of the Sei
whale. It is 9,8 cm long from basis to apex cordis and 9,2 cm widemeasured at the coronary sulcus. The left vagus, a 3,4 mm thickbundle descending down the neck, sends off, while it runs in front of
the aortic arch a remarkable branch (A) mediocaudally. This branch
makes its course to the right side always attached to the ventral surface of the aorta and reaches above the beginning part of the rightcoronary artery, where it communicates with a thick nerve (G) comingfrom the superficial cardiac plexus through the narrow space between
the ascending aorta and the pulmonary artery. This plexus is built
by the left sympathetic branches (B + C) and by the right vagosympathetic
nerve (D). These nerves have reached here from both sides passing
almost all behind the aorta. From the confluent nerve bundle (A+ G)
many branches are given to the ventral surface of the right ventricle inclusive of the conus arteriosus, all of them running downwards directly
under. the epicardium. From the complicated form of the plexus it isin this heart difficult to know, how much G conveys fibers from theright or from the left side.
The left sympathetic nerve, B and C, start from the trunk at avery high level, probably from the superior cervical ganglion anddescend for the greatest part behind the aorta. Only a very small
portion runs anterior to this vessel. Therefore, in comparison with
Berardius, one might conceive almost all of them as belonging to B.
B and C are divided into several branches in front of the right_ pulmonary artery dextral to the Botallo's duct, some of them making
ansae with each other, and most of them being united to the rightnerves (D). One small branch of B and C shows a very noteworthy
course (b). It passes at first in front of D to the right side, reaches
the left concave surface of the ascending aorta and goes then further
down passing behind D to the lower part of the anterior surface ofthe left atrium, where it unites with the most sinistral branch of D
(fig. 4 a, b). It is probable that fibers of this small branch are distributed to the lateral marginal part of the left ventricle.
D lies behind the aorta as a very thick nerve arising from theright side. It is made by union of Dr and D 2 • Dr comes out from thelower end of the right superior cervical ganglion, so is sympathetic innature, while D2 , certainly vagosympathetic, is much larger and starts
from the right vagus at the same level as the recurrens, but separately

'I'. OGAWA

from this. Just after confluence of D1 and D2 a remarkable branch is
given off from the dorsal part of D to the anterior surface of theright atrium (*1). This branch seems to bring the fibers corresponding
to the anterior branches of D5 and D6 of Berardius, considering thedestination of the fibers.
Superior
cervical

Right
vague

Left

,~,.,~~L

Fig. 4. Cardiac nerves of Balaenoptera
borealis (anterior view)Fig. 4 a. The nerve
plexus just behind
the aorta, in details·Behind the aorta the thick nerve D receives ·B and C from theleft side, but as C is minimal in this case, one can call hereafter the
resulted large trunk "B+D". From this B+D a thick branch (G)deviates to the right side, and connects with A, as already described.

Cardiac Nerves of Some Cetacea, etc.

13

It may be possible, though not fully proven, that G makes chiefly thecontinuance of B, as one can guess comparing the relation in this region
between Berardius and Balaenoptera.
Small ramuli are given off from G and from B + D to the hinder
circumference of the pulmonary ostium (fig. 4, *2, *3), to end probably
in a part of the conus arteriosus. B and D, or simply D if the analogy
with Berardius holds true, descend obliquely behind the stem of thepulmonary artery to the left side and reach after ramification partly
the anterior interventricular groove and partly the coronary sulcus.
The fibers are followed to the ventral wall of the left ventricle. It
seems that none of them goes from here to the right ventricle, butmany fine anastomoses are seen between nerves of the right and left
ventricles on the ventral surface.

Fig. 5. Cardiac nerves of Balaenoptera borealis (posterior view)
Rpa·. ·Right pulmonary artery
Ivc· ··Inferior vena cava
Cs .. · ·Sinus coronarius

Corresponding to D4 , D5 , D6 , D1, Ds, D9 of Berardius, the feta! heartof Balaenoptera has only two nerves, or better to say three, if one
adds the branch of D going to the anterior surface of the right atrium.
The two nerves might be called here DH and D6-9. D4-5• sympathetic

14

T. OGAWA

in nature, descends along the posterior and left surface of the superior
vena cava, and is distributed mostly to the atrial wall sinistral to thisvein, a few of its branches extending further into the right lung.
DH arises from the right vagus a little below the recurrens andgoes down the lateral surface of the right bronchus. Above the right
pulmonary artery it is divided into two, one of which (fig. 5, *4) descends in front of this vessel, becomes attached to the surface of theatrial musculature, gives off many branches horizontally to this, andruns subepicardially on the right side of the inferior vena cava, reachingat last the medial part of the coronary sulcus, caudally to this vein.
On the way it receives a small branch, which is issued from the branchof D going to the anterior surface of the right atrium (*1), and comes
posteriorly after penetrating through the Bachmann's bundle. The
other branch (fig. 5, *5) of D6 _ 9 descends behind the right pulmonary
artery, undergoes an anastomosis with a branch of D4-5 and continues
downwards in the atrial 'septum, partially reaching the left side of theinferior vena cava. The bundle, which corresponds topographically tothe septal nerve of Berardius, is very poorly developed in Balaenoptera(S); also the nerve plexus is relatively better developed anterior thanposterior to the right pulmonary artery. As to the septa! nerve agreat defference is perceived between Berardius and Balaenoptera.
The presence of a large assembly of nerve bundles (F) along the
Marshall's vein is common to both whales in question. These bundles
come in Balaenoptera too from the left vagus and the left sympathetic.
The sympathetic nerves (F1) start from the stellate ganglion and fromthe 2. and 3. thoracic ganglia. They descend, making a large trunk,in front of the vagus stem and of the aorta, then anterior to the left
pulmonary artery and reach the angle between the left pulmonary veinand the left auricula, giving rise here to the plica nervina of Worobiew.
One branch is sent off from the left vagus at the level of the recurrens, to take part in the formation of F after passing behind thepulmonary artery. The bundles of F reach mostly the coronary sinus,
after giving some ramuli to the dorsal wall of the left atrium andto the marginal part of the left ventricle, and then innervate after
repeated ramifications the greater part of the dorsal walls of the rightand left ventricles. A portion of them. sinks deeply at the left side of
the orifice of the coronary sinus, to enter probably into connection withthe atrioventricular node. The septal nerve (S), lying sinistral to theinferior vena cava, is small and seems to come mostly from the left
vagus. It shows anastomosis with the long branch of D6 _ 9 (*4), which

Cardiac Nerves of Some Cetacea, etc.

15

attains here dextral to the inferior vena cava. The connection between
the nerves originating from the right side and the atrioventricular nodeis less marked than in Berardius, though two small twigs (fig. 5, *6)from the long branch of D6 _ 9 are tracable, sinking deeply at the rightside of the coronary sinus, to the direction of the Tawara's node.

Prodelphinus caeruleoalbus Meyen(Figs. 6 and 7)

The left vagus sends off mediocaudally a remarkable branch (A)at a level slightly above the aortic arch. It descends along the ventral
surface of the aorta and then unites with the left sympathetic nerves(B), which have reached here behind the aorta. These sympathetic
nerves are grouped into two (B1 and B2), both starting from the middle
cervical ganglion of the left side. A joins at first with the more lateralcoursing B1 , and then with the more medial running B2 •Rif;htvagus

Left

Middlecervico 1
ganglionFig. 6.

Cardiac nerves of Prodelphinus caeruleoalbus (anterior view)

The thus formed nerve (A+ B) unites then with a large trunk (D)coming posterior to the aorta from the right side. D starts from theright vagus a little above the recurrens. It must contain both vagal

16

T. OGAWAand sympathetic components. On its way D receives small sympathetic
ramuli not only from the right but also from the left side.
The large trunk (A+B+D) gives off a branch (G), which goes
through the narrow space between the ascending aorta and the pulmonary artery to the base of the right coronary artery. The larger
remaining portion of A+B+D descends obliquely behind the pulmonary
artery to reach partly the interventricular groove and partly thecoronary sulcus, and the fibers are distributed chiefly to the ventral
surface of the left ventricle. Only a very small portion attains thelower part of the ventral surface of the left atrium.

Fig. 7.

Cardiac nerves of Prodelphinus caeruleoalbus (posterior view)At the space between the aorta and the pulmonary artery each of
B11 B2 , and D dispatches a thin branch, in all three rami, which unite
together into a single trunk, proceeding forwards on the right side of
the Botallo's duct to the dextrocranial surface of the pulmonary artery.
This innervates probably the conus arteriosus of the right ventricle.
Some small branches issued forth from the left sympathetic descend
behind the aorta and innervate the ventral surface of the left atrium.

Cardiac Nerves of Some Cetacea, etc.

17

From the right vagus another remarkable branch, corresponding to
D4 _ 8 of Berardius, starts a little below the recurrens. It is about half
so thick as D, and is divided while descending into two, anterior andposterior. They go partly to the ventral surface of the right atrium,
partly behind the Bachmann's bundle just in front of the right pulmonary
artery to the septal raphe of Papez, but for the greater part behind
the right pulmonary artery, making here a thin but broad sheet ofnerve fibers closely attached to the dorsal surface of this vessel (fig. 7,*l); thence the fibers reach partly the septal raphe, partly the atrial
septum to continue further down into a remarkable septal nerve (S).
Just above the septal raphe, where many of the atrial musculatureshow the tendency to concentrate, we see well developed nerve plexuses.
To these the right vagal and sympathetic fibers are brought in by
D4 _ 8 , while the left vagal and sympathetic fibers are conveyed by anerve bundle (*2), which descends obliquely from upper left to lower
right directly behind the bifurcatio of the right and left pulmonary
arteries, and whose origins each from the left vagus and from the left
sympathetic are determined clearly. The vagal component (*3) comesfrom the base of the recurrens; the sympathetic one (*4) belongs to
the most sinistral bundles of B.
F is a large group of nerve bundles, running along the Marshall's
vein. It consists of the vagal and sympathetic fibers coming from theleft side. The vagal branch (*5) begins nearly at the same level as
the recurrens. Fibers of F are distributed partly to the dorsal wallof the left atrium, but for the greater part to the dorsal walls of theright and left ventricles. At the fossula nervina of Worobiew a partof F together with a portion of the septal nerve sinks deeply to thedirection of the Tawara's node.
Speaking in short, the cardiac nerves of Balaenoptera and Prodelphinus are considerably different from those in Berardius. In themthe crossing of the nerves going to the ventral walls of the ventricles is not so clearly seen, except as to the branch A in Balaenoptera,
which starts from the left vagus and innervates definitely a portionof the ventral wall of the right ventr!cle. In Prodelphinus even thevagal branch corresponding to A is lost in the superficial cardiac plexus,
so its further course, whether to the right or to the left ventricle,
is very difficult to ascertain. But the possibility, that also here thesame relation as in Berardius exists, should not soon be excluded. No
definite proof could be obtained against this assumption. I thought atfirst to have met such a proof in a small branch (b) of Balaenoptera,

18

T. OGAWAwhich belongs to the left sympathetic nerve and goes after a complicated detour to the left ventricle. But as its destination is certainly
the transitional part between the ventral and dorsal walls of the left
ventricle; this observation too never disproves the thesis.
The second problem, that the nerves ending in the atria and thedorsal walls of the ventricles start from the stems generally morecaudally than the nerves going to the ventral walls of the ventricles,
and moreover they are probably not crossing, holds also in Balaenoptera
and Prodelphinus, though in these Cetacea the cardiac nerves especiallyon the right side, which descend posterior to the transverse sinus, aregathered into a small number of trunks, 2 or 3, while in Berardius
the corresponding number is so large amounting to 10, that one canin this whale more easily determine the height of origin for each branch
innervating various parts of the heart.
The third problem is relative to the nerve plexus lying near theright pulmonary artery just above the concentration area of the atrial
musculature and to the septal nerve descending through the atrial
septum. Concerning them there is a great difterence between thetoothed whales, Berardius and Prodelphinus, and the baleen whale,
Balaenoptera. In the former the nerve plexus in question is very welldeveloped and branches from the vagus and sympathetic of both sides
are clearly traced to this plexus and an imposing septal nerve descends
passing sinistral to the inferior vena cava toward the fossula nervina.
Contrarily, the nerve plexus surrounding the right pulmonary arteryas well as the septal nerve is meagre in Balaenoptera. Instead of the
septal nerve, the Sei whale has a large nerve, which departs from theright vagus and descends on the dorsal surface of the right atrium passing dextral to the inferior vena cava.
To the Tawara's node the left nerves go mostly through the nerve
bundles running along the Marshall's vein and the right nerves chiefly
through the septal nerve. These relations are seen well in the toothed
Cetacea, while in the Sei whale the nerve descending right to theinferior vena cava seems to substitute for the septal nerve, as to theinnervation of the atrioventricular node.
Comment

It was a much impressive observation in the fetal heart of Berar-

dius, that the cardiac nerves leaving the vagus and the sympathetic at
relatively high levels to innervate the ventral walls of the ventricles
decussate for the greatest part, and the present author does not take

Cardiac Nerves of Some Cetacea, etc.

19

this fact for a mere variation or a characteristic feature restricted
only to this species. It seems to have more important significance.
Up to the present time the crossing of the cardiac nerves has
been very few spoken of. Kazem-Beck saw in 1888 in the rabbit
branches of the superficial cardiac plexus, especially those coming fromthe left cardiac ramus, go between the aorta and the pulmonary arteryto the surface of the right ventricle. Moreover, in some rabbits KazemBeck found that the left cardiac ramus, before it undergoes connection
with the right nerves, sends off a twig, which goes along the pulmonary
artery to the surface of the ventricle. By this "ventricle" he musthave meant the right one, as we can estimate from his figure andexplanation (fig. 1 d of his paper). Also in the dog's heart Kazem-Becktraced a portion of fibers, which belong mostly to the right cardiac
rami, from the plexus to the surface of the left ventricle. Per haps
he was of the opinion, that not a small amount of the cardiac nerves
are crossed in these animals, though he did not emphasize at all upon
the decussation.
On the contrary, Schumacher (1902) concluded in his extensive studies
on many mammalian hearts, that the right nerves innervate in general
the right atrium and the right ventricle, including a part of the left
ventricle adjacent to the anterior interventricular groove, while theleft nerves are distributed solely to the left ventricle and the left
atrium. The remarks of Schumacher seem to have found relatively
much agreement in the successors. Meanwhile Perman (1924) proposed
partial correction of Schumacher's conclusion, though he acknowledged
also the ipsilateral relation for the most of the cardiac nerves. In
several mammals Perman could trace one or two nerves coming fromthe left side and passing anterior to the aortic arch, to the right ventricle.
My own acquisition in Berardius looks quite extraordinary in thisrespect. But to my mind the more general occurrence of the contralateral relation for the cardiac nerves is never inconceivable, if one
considers that in most mammals through the inextricable maze of thesuperficial cardiac plexus each nerve bundle can never be persued withconfidence. The difficulty of tracing them confidently through the plexus
was great also in Balaenoptera and Prodelphinus, and thereupon theunique finding in Berardius, in which only minimal anastomosis takes
place between the nerves of both sides, seems to mean much.
The decussation of the cardiac nerves above ref erred to was caused
in my opinion by the torsion of this part of the ventricular canal, whichmust have occurred in the early embryo in the region of the porta

20

T. OGAWAarteriosa. Braus wrote in his famous textbook, "eine Torsion desHerzschlauches in der Nahe der Porta arteriosa mit dem Uhrzeiger(von der Arterie stromaufwarts gesehen)-auch an Einrichtungen desmenschlichen Herzens erkennbar." (H. Braus : Anatomie des Menschen.
Bd. 2, 1924, S. 626) Our finding tells probably, that the musculatureof the ventral wall of the right ventricle was given rise at first on
the left side, and that of the ventral wall of the left ventricle on theright side, the nerves retaining their original relation honestly till theadult stage.
A natural deduction from this is my rather bold assumption, thatthe neuromuscular connection must have begun in the heart very early,
though since His jr. (1891) the late innervation of the heart has often
been reported. In the fowls' heart His jr. saw the first nerves appear
on the 6. day of incubation, and Perman (1924) observed them in theembryo of 4 days and 2 hours. As to mammals, Hall (1951) met withnerve fibers in the sinus venosus and atria only of the rat embryos
older than 14,5 day stage, a remark which sounds not a little contradictory to the earlier work of Shaner (1930), who proved the presenceof all nerves going to the heart of a 20 mm long calf embryo already.
Anyway, the relatively late development of the cardiac nerves has
furnished, as well known, the most powerful basis for the myogenic
theory of the conduction or automatism in the cardiac function.
My hypothesis upon the early innervation of the heart finds, however, another support in the fact, that the nerves entering the superficial cardiac plexus, which corresponds undoubtedly to the "Bulbusgeflecht" of His jr., start from the vagus and sympathetic at levels
generally higher than the nerves descending posterior to the transverse
sinus to both atria and to the dorsal walls of both ventricles. The
nervous connection of the heart seems to have been established in avery young embryo, when the porta arteriosa was situated more rostrally
than the porta venosa. Otherwise, the above mentioned difference ofthe levels, where the cardiac nerves leave the vagus and sympathetic
trunk, might be difficult to explain.
Another finding, that in Berardius the conus arteriosus of the rightventricle receives a special innervation, viz. chiefly the most rostral
sympathetic fibers coming from the left side, deserves also much attention from the embryological viewpoint, as this part is generally looked
upon as nothing than the bulbus arteriosus of the early embryo.
As to the problem of the cardiac nerves the sinus node discoveredby Keith and Flack seems to be in the Cetacea no special locality, asCardiac Nerves of Some Cetacea, etc.

21

only a few small branches of the right nerves reach there. Contrarily
a remarkable nerve plexus, especially well developed in the toothed
whales, is attached to the atrial wall just dextral to the interatrial
septum and directly under the right pulmonary artery. Papez named
this portion ''septal raphe'' and called attention to the richness ofnerves coming there from the right vagosympathetic. I myself could
observe in addition branches from the left vagus and from the left
sympathetic reaching distinctly the nerve plexus in question.
Summary

The cardiac nerves were studied with naked eye in the f etuses ofBerardius bairdii, Balaenoptera borealis and Prodelphinus caeruleoalbus.
In Berardius the vagal and sympathetic nerves originating from theright and left side and attaining the ventral walls of the ventricles
decussate at least for th~ most part, the left nerves going to the right,
the right ones to the left ventricle. In Balaenoptera and Prodelphinus
the decussation of these nerves is not definitely determined, though its
possibility can also never be denied. They start from the vagus andsympathetic trunk always more rostrally than the other nerves, which
descend posterior to the transverse sinus to both atria and to the dorsal
walls of the ventricles. For the latter the ipsilateral innervation, theright to right and the left to left, probably prevails.
We may explain these findings the most easily from the complicatedmorphogenesis of the mammalian heart, but at the same time we haveto assume the very early innervation of the heart musculature, a fact,which does not coincide well with the data reported by previous authors.
Innervations of the sinus node, of the Tawara's node and of the septal
raphe of Papez were also studied, special attention being paid to the septa!
nerve, which descends through the atrial septum, and to the thicknerve bundles, which run together with the Marshall's vein. A great
difference was recognized as to the development of the septal nerve
between the toothed whales and the Sei whale.
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T. OGAWA

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From the Departm@nt of Anatomy (Prof. Dr. T. Ogawa)
Medical Faculty, University of Tokyo