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ABSTRACT
Anatomy of the cardiac conduction system was studied in 15 rabbits with
serial histologic sectioning of 4. The rabbit's sinus node is a simple and dis-
tinct structure located at the junction of the crista terminalis with the sinus
intercavarum nearly midway between the two cavae; it contains an unusually
large percentage of P cells but is not organized about a large central artery. The
AV node and His bundle are relatively small and are displaced anteriorly by
the large coronary sinus normally present in the rabbit because of its persisting
left superior vena cava. The AV node is organized with input system and by-
pass tracts similar to those of man and the dog. Doth the AV node and His
bundle contain many conspicuously large nerve trunks. The blood supply of the
sinus node is from terminal small branches of both the right and left coronary
arteries and that to the AV node and His bundle is from similar terminal
branches of the septal artery only. The possible functional significance of some
of these anatomic features is discussed.
• Rabbits are frequently utilized in experi- tion system in human (8-12), canine (12-14)
ments on cardiac electrophysiology, and and bovine (15) hearts.
many of the most important recent observa-
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parallel to the junction of interatrial and in- to transitional or ordinary working myocardial
terventricular septa, and perpendicular to the cells in the rabbit's sinus node is exception-
plane of the diaphragmatic surface of the heart. ally high. These cells are round or oval, occur
A second orienting cut was made perpendicular
to the first one and passing through the anterior in chains or clusters, contain relatively few
margin of the main pulmonary artery and the myofibrils (which are randomly oriented in-
crista supraventricularis. The principal purpose stead of parallel to each other), and are
of the second cut was to orient the specimen for thought to be the site of pacemaking within
the start of serial sectioning. In all specimens the node (6, 7, 12). The two other cell types
this orienting cut proved to be anterior to any
recognizable bundle branches. This block of tis- are scattered, ordinary working myocardium,
sue, comprising more than half of the heart, was which is distributed mainly (but not exclu-
then embedded in paraffin and cut serially at sively) at the margins of the node, and a
6-fi intervals. Of these sections 2 successive ones group of transitional cells with internal fea-
of every 20 (nos. 1, 2; 20, 21) were mounted. tures intermediate between the simple pale
The stain routinely employed was the Goldner
modification of the Masson trichrome, but in se- P cells and the dark staining working myo-
lected specimens intervening sections were stained cardium. The distribution of P cells was rath-
for elastic tissue or other special structures. er homogeneous for the length of the node.
The margins of the rabbit's sinus node are
Results unusually distinct and this is attributable to
General Topography of the Conduction the large percentage of P cells, making the
System.—The sinus node of the rabbit is lo- contrast with ordinary atrial myocardium
cated nearly midway between the ostia of the more apparent. The sinus node of the rabbit
right superior vena cava and the inferior vena is not organized about a central ajtery but
cava, just beneath the epicardium of the junc- contains only small arterial branches of a
tion of crista terminalis and sinus interca- size appropriate for a nutrient function alone.
varum (Fig. 1). Since the rabbit normally The course of the left superior vena cava
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has a left superior vena cava (16, 17), the over the left atrium was carefully examined
ostium of the coronary sinus (embryolog- for nodal tissue, since it is both an anatomic
ically derived from the terminal portion of the and an embryologic counterpart to the right
left superior vena cava in most mammals) is atriocaval junction. Myocardium in the wall
unusually large. This effectively displaces the of the left superior vena cava is inseparable
AV node and His bundle anteriorly toward from that of the left atrium and no collagen
the root of the aorta. The large ostium of the nor any other plane of cleavage was ob-
coronary sinus also alters the size and dis- served. At variable locations there were small
tribution of the intemodal tracts, as discussed clusters of pale cells, but under higher mag-
later. nification (light microscope) these were not
The Sinus Node.—This loosely organized the same as P cells of the sinus node, resem-
structure occupies the entire thickness be- bling more the transitional cells. On an ana-
tween endocardium and epicardium at the tomic basis, no centers (nodes) similar to
junction of the midportion of sinus interca- those with known spontaneous pacemaking
varum and crista terminalis, and is oblong activity could be identified along the junction
with its long axis parallel to the crista ter- of the left superior vena cava with the left
minalis (Fig. 2). Its total length varied from atrium. The same was true of junctions be-
500 to 800 fi. There is relatively little collagen tween pulmonary veins and the left atrium.
in the rabbit's sinus node. The cells are or- The AV Node.-The AV node lies just be-
ganized into interweaving fibers and are neath the right atrial endocardium anterior
easily differentiated from ordinary atrial myo- to the ostium of the capacious coronary sinus
cardium by their smaller size and paler stain- and above the septal insertion of the tricuspid
ing as well as by the difference in organiza- valve (Fig. 4). Because the ostium of the
tion (Fig. 3). The proportion of P cells (12) coronary sinus is so large in the rabbit, the
Circulation Rttaircb. Vol. XX, /»»# 7967
640 JAMES
FIGURE 1
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FIGURE 2
Circulation Rtsetrcb, Vol. XX, ; » « 1967
ANATOMY OF THE RABBIT HEART 641
Nerve trunks are impressively large and eas- The node is between the two arrows in A, where the
ily identified in the AV node of the rabbit, comparative difference from ordinary atrial fibers is
apparent. Cells of the sinus node are shown in B at
from which they course into the His bundle. higher magnification. The reference bar in each repre-
The anatomic input system of the AV node sents 0.1 mm.
from the atrial septum may be divided into
two general regions, that of the superior and Those fibers which pass the nodal crest and
posterior crests of the node and that along its course beneath the right atrial endocardium
right atrial surface. Atrial septal cells forming to enter the node at its more distal end near
these two input regions arrange into fibers the junction with the His bundle are identi-
which intermingle at the nodal margins. cal to similar anatomic "bypass" tracts de-
Fig. 1.—Rabbit heart fixed in formalin with blood remaining in the chambers, thereby preserving its normal shape. A
is a view over the right atrium (RA). The crista terminalis is seen as a pale band lying between the free wall of atrium
and superior vena cava (SVC). The approximate location of the sinus node is indicated by the arrow. B is a view of
the posterior surface of the same heart to demonstrate the normal large left superior vena cava which terminates
as the coronary sinus (CS). Left and right ventricles are labeled LV and RV.
Fig. 2.—Low-power photomicrographs of the sinus node from two rabbits. The 1-mm reference bar indicates the
same magnification for both A and B. The sinus node extends throughout the thickness of the section in the area
between the two open arrows, which are placed on the epicardial surface. In each section the free wall of right
atrium extends to the left and the wall of the sinus intercavarum extends to the right. The large mass of myo-
cardium in each is a cross section of crista terminalis.
CircmUlion Rts—nb, Vol. XX, J*»i 1967
642 JAMES
FIGURE 4
A, sections through the AV node and B, the commencement of the His bundle. These are from
the same heart and the distance between the two sections is approximately 1.8 mm, B being
anterior to A. In each, the interventricular septum is below and to the right, with atrial septum
above; the right atrial cavity is to the left in the photographs; the 0.5-mm reference bar indi-
cates the same magnification in both. In A the AV node is seen in cross section at approxi-
mately its maximal size, lying between the two arrows. Larger fibers of the bypass tract lie
between the node and right atrial cavity, coursing beneath the endocardium and connecting
with the AV nodal fibers along the right atrial surface of the node; the central fibrous body is
along the right upper margin of the picture. In B the His bundle (arrows) is shown separated
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from the atrial septum above by collagen, as it courses to its tiltimate position at the crest of
the ventricular septum.
scribed in other species (9, 14, 15). The dle organize into more longitudinally oriented
minimum thickness of the bypass tracts fibers which are generally of larger dimension
measured perpendicular to atrial endocardium than those of the two nodes, but this dimen-
(and the corresponding surface of the AV sion is not consistent, some of the fibers being
node) is 50 to 150 /x. The cells in the bypass smaller. The region of membranous interven-
tract in the rabbit are larger than those of the tricular septum so conspicuous in many mam-
AV node but stain paler than those of or- mals is barely identifiable separate from the
dinary atrial myocardium. The only arteries central fibrous body in the rabbit. The length
in the AV node are small branches of a size of the His bundle through the central fibrous
suitable for nutrient supply. body before the bundle branches is less than
The His Bundle.—Continuing from the an- 200 yx. Its shape on cross section is oblong,
terior and inferior margin of the AV node, with the larger dimension (about 150 (JL) be-
the His bundle descends through the central ing lateral. The total length of anatomically
fibrous body to the crest of the ventricular identifiable undivided His bundle in the rab-
septum, where it begins to divide into a sheet bit is thus remarkably small. Beginning with
of left bundle branches and a slender, small left bundle branches, the length of the His
right bundle branch. The impressively large bundle continues 100 to 200 /x, and in this
and easily identified nerve trunks of the AV course, at variable points of departure, the
node continue through the His bundle (Fig. right bundle branch originates. The maximal
5) and then become more difficult to identify dimension on cross section of the right bundle
in the bundle branches. Cells of the His bun- branch near its origin is about 40 /x. While
Circulation Rcsurcb, Vol. XX, Jum 1967
ANATOMY OF THE RABBIT HEART 643
FIGURE 6
Coronary arteries of the rabbit heart. This and the photographs in Figures 7 and 8 are all
of the same heart, which was prepared by injection of barium gelatin into the root of the
aorta and then clearing of the specimen in oil of wintergreen. In A the typical course of left
coronary artery is shown, with the major mural branch indicated by the short white arrow.
Next to it toward the right ventricle (RV) is a branch coursing within the myocardium in the
interventricular septal sulcus, and thus corresponding to the human anterior descending ramus;
this branch is not large in the rabbit. The next two branches are both over the right ventricle
but originate from the branch in the anterior interventricular sulcus; the one corresponding
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to the conus artery in man is indicated by the enclosed black arrow. A long thin branch of
the main left coronary trunk (which corresponds to a diagonal left ventricular artery in man)
is seen coursing between the left ventricle (LV) and the body of the left atrium (LA), cor-
responding roughly to the human left circumflex branch, although it courses below the AV
stdcus. The final important branch in A is the left atrial artery indicated by the thin arrow
as it leaves the left coronary to course beneath the left atrial appendage and enter Bachmann's
bundle.
In B the heart has been rotated so the main left coronary trunk (short white arrow) courses
along the right margin of the heart, and the conus artery over the pulmonary conus is indicated
by the short enclosed black arrow. The main right coronary artery (long arrow) is seen coursing
over free wall of the right ventricle (RV) below the AV sulcus, with only a small branch lying
in the stdcus between the ventricle and the right atrium (RA); this small branch corresponds
to the usuil location of the main right coronary artery in man. The rule in Figures 6-8 = 1 cm.
pass beneath the ostium of the coronary sinus and corrosion. The rabbit has a right and left
(localized electrophysiologically by Paes de coronary artery, but most of the heart is sup-
Carvalho and associates (5) are only a few plied by the left coronary and its branches
cells in cross section. By contrast, the fibers (Figs. 6, 7). In addition to those branches
constituting the anterior internodal pathvvav which supply the free wall of left ventricle,
form large bundles which are easily dissected the left coronary artery consistently provided
grossly. a large septal branch similar to that of the
The Coronary Arteries.—With the method dog (19). Unlike the pattern in the dog, how-
employed in this study, the distribution of the ever, a major left ventricular branch does not
coronary arteries in the rabbit was found to course to the crux of the heart in the rabbit,
be similar to that described by Day and nor is there a posterior descending artery.
Johnson (18) from studies utilizing injection Other important distinctive features of the
Circulation Ruttrcb, Vol. XX, Jmm 1967
ANATOMY OF THE RABBIT HEART 645
FIGURE 7
The lateral and posterior surfaces of the right ventricle and atrium are shown in A, including
the distal distribution of the right coronary artery, the only major vessel visible; there are two
small atrial branches. The asterisk indicates the poorly vascularized region of the crux. In B
the heart -is-viewed_directly from above, demonstrating the origin of the right (R) and left (L)
coronary trunks from the root ~of~the~aorta -(Ao). The undivided proximal portion of the left
coronary artery is obscured here but well shown in Figure 6A. The left atrial artery is indicated
by the arrow.
origin, branches from the septal artery are certain important anatomic differences. There
perpendicular to its long axis and ascend are a sinus node, intemodal pathways, AV
across the right ventricular septal endocar- node, His bundle and bundle branches in the
dium to reach the His bundle and then the rabbit. The differences from the other species
AV node (Fig. 8). This sequence of arterial concern their internal organization, topograph-
penetration is opposite to that in man, in ical location in the heart, relative sizes, and
whom the blood supply of this region enters the origin and distribution of their arterial
from the posterior margin of the AV node blood supply.
after originating at the crux (9, 19). In the The sinus node of the rabbit is relatively
dog, the blood supply of this same region is long, considering total heart size, and it is
dual from the posterior and anterior mar- unusually far posterior on the line from su-
gins (14, 19), and thus resembles that of perior to inferior vena cava, but the two
both man and the rabbit. To understand this most impressive anatomic features concern
particular void in arterial distribution to the its internal structure. It contains an inordi-
region of the crux of the heart of the rabbit, nately large percentage of P cells, and it is
it should be kept in mind that a left superior distinctly not organized about a central ar-
vena cava is normally present, the coronary tery. The percentage of P cells is probably
sinus consequently very large, and most atrial comparable to that of the steer, but consider-
septal structures (including the AV node) ably greater than that of either dog or man.
displaced anteriorly away from the epicar- What this signifies concerning pacemaking
dium of the crux. potential in the rabbit heart is uncertain, but
Day and Johnson described only one con- it should be simpler to locate pacemaking
stant atrial artery in the rabbit, arising from cells with an exploring microelectrode in
the left circumflex branch (Figs. 7B, 8A), the rabbit than in the dog. In attempting to
with no large or constant atrial branches of predict the precise location of pacemaking, it
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the right coronary artery. In the present study would be helpful anatomically if a larger con-
the presence of the left atrial artery was centration of P cells were present at the an-
confirmed, as was the absence of any sizable terior or posterior margin of the rabbit's sinus
right atrial arteries. The left atrial artery node, but this is not the case. Functionally, of
coursed beneath the atrial appendage to en- course, any portion of the node may predom-
ter Bachmann's bundle, but by that point inate for pacing, despite the anatomic homo-
it had already divided into at least two small- geneity.
er branches. In no specimen did this artery In man and the dog the sinus node is dis-
continue as a large trunk to the region of the tinctly organized about a conspicuously large
sinus node, although its terminal branches centrally located artery, but not in the rabbit
appeared to supply that region. Other smaller (or the steer). There is some physiologic
atrial arteries ascended toward the crista ter- evidence that pulsations of the sinus node ar-
minalis from the proximal right coronary ar- tery may influence the rate of pacemaking by
tery, but the distal right coronary was too far the cells of the sinus node in the dog (20-23),
from the AV sulcus to provide any significant acting as a stabilizing feedback signal or
atrial branches. In no specimen studied was servomechanism. If this is true, then the sinus
there a grossly visible atrial artery in the node of the rabbit may function as a less
region of the sinus node, although small ones stable pacemaker. The possibility is support-
could be identified in the histologic sections. ed by the well-known instability of sinus
pacemaking in the intact rabbit, particularly
Diicustion when unanesthetized.
In the rabbit heart the conduction system Both the AV node and the His bundle as
is organized in a pattern generally similar to anatomically defined are relatively small in
that of the steer, dog, and man, but there are the rabbit. This may be in part due to the
Circulation Rtsnrcb, Vol. XX, Jmif 1967
ANATOMY OF THE RABBIT HEART 647
foreshortening of the entire area produced by the possibility exists of better conduction
the presence of the large ostium of the cor- through smaller anatomic paths. Present phy-
onary sinus, which drains not only the cardiac siologic evidence indicates there is more
veins but the normally present left superior rapid conduction through the lapine anterior
vena cava. Despite its small size, the AV and posterior intemodal pathways (25) than
node of the rabbit is organized like that of in ordinary myocardium, although not as rap-
man, dog, and the steer. There is no os cordis id as that in the His bundle. This would be
of the type found adjacent to the AV node predictable on the basis of a smaller percent-
and the His bundle in the bovine heart (15). age of cells with Purkinje or specialized char-
The similarity of AV nodal organization in- acteristics in the intemodal pathways than in
cludes the input system at the nodal crest and the His bundle. However, one may anticipate
the presence of anatomic bypass tracts. For that the speed of conduction in the intemodal
considerations of function of the AV node pathways would be slightly greater in the
and His bundle, one may question the "ma- rabbit than in man or the dog, since the pro-
turity" of this region in the rabbit because of portion of specialized cells in the rabbit seems
the normal presence of the left superior vena greater. In all three species, the speed should
cava. Patten (24) has suggested that the em- still be greater in intemodal paths than in
bryologic origin of the AV node is from the ordinary myocardium. Rapid conduction has
junction of the left superior cardinal vein been demonstrated in one region of the pos-
with the sinus venosus, in a position identi- terior intemodal pathway of the rabbit (5)
cal to that of the sinus node at the junction of which is at least partially diverted beneath
the right superior cardinal vein and the sinus the coronary sinus instead of over it as in
venosus. As the sinus venosus is normally the dog or man. This minor anatomic differ-
absorbed into the atria in most mammals, ence may be attributable to the size of the
the left superior vena cava is incorporated rabbit's coronary sinus.
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8. JAMES, T. N.: Anatomy of the human sinus casional peculiarities in the human subject.
node. Anat. Record 141: 109, 1961. Phil. Trans. Roy. Soc. London 140: 133,
9. JAMES, T. N.: Morphology of the human atrio- 1850.
ventricular node, with remarks pertinent to 17. CRAJCIE, E. H.: Bensley's Practical Anatomy of
its electrophysiology. Am. Heart J. 62: 756, the Rabbit, 7th ed. Philadelphia, Blakiston,
1961. 1957.
10. JAMES, T. N.: The connecting pathways between 18. DAY, S. B., AND JOHNSON, J. A.: Distribution of
the sinus node and the A-V node and between the coronary arteries of the rabbit. Anat. Rec-
the right and the left atrium in the human ord 132: 633, 1958.
heart. Amer. Heart J. 66: 498, 1963. 19. JAMES, T. N.: Anatomy of the Coronary Ar-
11. JAMES, T. N., AND SPENCE, C. A.: Distribution teries. New York, Paul B. Hoeber, Inc., 1961.
of cholinesterase within the sinus node and 20. JAMES, T. N., AND NADEAU, R. A.: Sinus brady-
AV node of the human heart. Anat. Rec. 155: cardia during injections directly into the sinus
151, 1966. node artery. Am. J. Physiol. 204: 9, 1983.
12. JAMES, T. N., SHEBF, L., FINE, C , AND MOR- 21. JAMES, T. N., AND NADEAU, R. A.: Study of
ALES, A. R.: Comparative ultrastructure of the retrograde pressure and pulse in the sinus
sinus node in man and dog. Circulation 34: node artery. Am. Heart J. 66: 343, 1963.
139, 1966. 22. JAMES, T. N., AND NADEAU, R. A.: Relation
13. JAMES, T. N.: Anatomy of the sinus node of the of retrograde pressure in the sinus node artery
dog. Anat. Record 143: 251, 1962. to sinus tachycardia from stellate stimulation.
14. JAMES, T. N.: Anatomy of the A-V node of the J. Lab. Clin. Med. 62: 777, 1963.
dog. Anat. Record 148: 15, 1964. 23. JAMES, T. N., AND NADEAU, R. A.: Effects of
15. JAMES, T. N.: Anatomy of the sinus node, AV vagal stimulation, eserine and atropine on
node and os cordis of the beef heart. Anat. retrograde pressure in the sinus node artery.
Record 153: 361, 1965. Henry Ford Hosp. Med. Bull. 12: 23, 1964.
16. MARSHALL, J.: On the development of the great 24. PATTEN, B. M.: The development of the sino-
anterior veins in man and mammalia: In- ventricular conduction system. Univ. Mich.
cluding an account of certain remnants of Med. Bull. 22: 1, 1956.
foetal structures found in the adult, a com- 25. SANO, T., AND YAMACISHJ, S.: Spread of excita-
parative view of these great veins in the dif- tion from the sinus node. Circulation Res.
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