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A comparative morphologic study of the cardiac innervation in domestic animals II. The feline

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A Comparative Morphologic Study of the Cardiac
Innervation in Domestic Animals
11. THE FELINE
JOHN SCOTT McKIBBEN AND ROBERT GETTY
Department of Veterinary Anatomy, Iowa State University, A m e s , Iozua
ABSTRACT
Detailed morphological studies of the cardiac innervation of the cat
were reported. Sympathetic cardiac nerves arose from the thoracic, cervicothoracic,
vertebral, and intermediate ganglia. Parasympathetic cardiac nerves arose from the
vagi, both cranial and caudal to the origin of the recurrent laryngeal nerves, and
from the right recurrent laryngeal nerve. Left cardiac nerves passed primarily to the
caudal and right surfaces of the left chambers while right ones ramified on the right
chambers and left portion of the left chambers. Left cardiac nerves are more prominent around the coronary sinus and atrioventricular node, while right ones contribute
more to the area of the sinoatrial node. Both sympathetic and parasympathetic nerves
were followed to each chamber. Interconnections through the cardiac plexus facilitated overlapping of nerve distributions.
The cat, although having an early history as an animal for various laboratory
investigations, has not enjoyed the attention of cardiologists which the dog has received. Anatomical descriptions of the cardiac innervation are limited. Bernhardt
(1868), Boehm (1875), and Kazem Beck
(1888) described the depressor nerve and
its relationship to the heart. Mannu ('14)
reported on the cardiac nerves of one cat.
Perman ('24), Nonidez ('39), and Saccomanno ('43) contributed further information regarding the cardiac innervation
of the cat. Only Anufriew ('28), however,
has morphologically described the innervation of the feline heart in detail.
Current veterinary anatomical textbooks
do not include the morphological description of these cardiac nerves in the cat. The
present investigation includes further morphological observations relevant to the
proper understanding of cardiac function
as well as for specialized procedures such
as cardiac denervation studies.
MATERIAL AND METHODS
Ten adult cats were embalmed using
the Iowa State University, Department of
Veterinary Anatomy embalming formula.
Direct morphologic dissection proceeded,
exposing and tracing the cardiac nerves,
as previously described (McKibben and
Getty, '68).
AM. J. ANAT., 122: 5 4 5 5 5 4 ,
RESULTS
A. Thoracic ganglia and cardiac nerves
Independent THORACIC GANGLIA were
present along the thoracic sympathetic
trunks bilaterally in each intercostal space
from the third or fourth space caudally.
They maintained a fairly uniform size of 2
mm craniocaudal, 1 mm dorsoventral, and
1 mm mediolateral. LEFT thoracic cardiac
nerves arose from the third to fifth thoracic
ganglia, joined the dorsal cervicothoracic
cardiac nerve and entered the cardiac
plexus. RIGHTthoracic cardiac nerves passing directly to the heart were not observed
grossly; however, nerves arising from the
third and fourth thoracic ganglia joined
the right vagus nerve and potentially could
reach the right atrium with the right caudal vagal cardiac nerves.
B . Cervicothoracic ganglia and
cardiac nerves
On each side the CAUDAL CERVICAL and
first two or three THORACIC GANGLIA combined to form the CERVICOTHORACIC GANGLION.This ganglion lies on the lateral surface of the longus colli muscle in the first
intercostal space on the right side, and extends between the first and second intercostal spaces on the left side. Rami communicantes extend caudally at least to the
third thoracic spinal nerve and cranially
545
Feline Approximate
feline
Left
number weight
8
8
7
8
9
10
2
4
4
9
7
8
Average8
8
5
7
4
4
4
4
5
5
4
5
4
D-V
8
6
7
7
6
8
7
9
6
6
C-C
2
3
1
1
1
1
2
unidentified
4
3
2
3
1
1
Grossly
Grossly
unidentified
Grossly
unidentified
unidentified
unidentified
Grossly
Grossly
unidentified
Grossly
unidentified
Grossly
Grossly
unidentified
Grossly
Grossly
unidentifies
Grossly
unidentified
unidentified
0.50.50.5
Grossly
unidentified
unidentified
Grossly
Grossly
Grossly
unidentified
n4-I.
unidentified
unidentified
1
Grossly
C-Ti
Unidentified
M-L C-C
unidentified
0.50.50.5
Grossly
D-V
Intermcdiate
ganglion
Riglit
Grossly
Grossly
1
1
1
1
1
1
1
1
2
1
1
1
M-L C-C
Left
unidentified
6
3
4
2
2
3
1
1
D-V
Right
Ansa subclavia 1
Left
Right
length
length
10
10
15
12
15
5
8
8
7
10
10
19
25
30
18
20
15
15
12
10
20
23
17
13
20
30
13
20
13
15
10
20
20
28
23
35
45
20
30
20
25
20
30
30
~-
Cranial Caudal CranGal Caudal
limb
limb
limb
limb
The width of th& cradial limbs aver'aged hne half millimeter: usually double caudal limbs averaged, together, 1 mm in width.
1
1
1
1
1
unidentified
2
1
1
1
2
Grossly
2
1
1
1
1
4
4
4
3
3
1
3
unidentified
3
1
1
2
2
M-L C-C
Vertebral
ganglion
Grossly
I>-V
Left
2
2
1
2
2
2
2
2
M-L C-C
C-C Craniocaudal. D-V Dorsoventral. M-L Mediolateral.
2
2
5
7
8
2
2
4
4
2
2
2
2
2
2
M-L
Cervicothoracic
ganglion
Right
7
7
8
8
6
4
4
5
3
10
8
4
5
4
8
8
3
7
4
4
8
2
6
D-V
6
8
1
pounds C-C
in
TABLE 1
Feline: dimensions o f the ansa subclavia an,d of t h e ganglia o j origin f o r cardiac nzrves in millimeters
221-1
2
M
2
9
*3
E3
m
r-1
I-1
82
rn
8
cl
+,
Left
Right
Left
Right
Left
Right
Left
Right
Left
Right
Left
Right
Left
Right
Left
Right
Left
Right
Side
-
-t+,
++
+
+
+
++
+
+
++
+
+
++-
right
coronary
artery 1
+
++++
+
+
+
++-
-
I-
++
++
Along the
descending and
circumflex
branches of
the left coronary artery
on the left
bid? 2
+++,
Along the
circuinflex
branch of
the left coronary artery
caudally and
on the
right sides
Between the
cranial and
caudal venae
cavae 4
Between the
caudal vena
cava and
le€t atrium 6
-
++
+
++
++++
+
++
++
+++
++-
+
Cardiac
plexus 6
-, not followed to this area;
some may supply this area;
moderate supply to the area;
major supply to the area.
1 Main distribution includes the right aupcle, atrium, “d
ventncle.
ZMain distribution includes the left auricle left ventricle on the left side left interventricular septum and the left cranial portion of the right ventricle.
3 Main distribution includes the dorsum of ’the left auricle, ventrum of tlk left atrium, caudal and right sides of the left ventricle, right interatrial and
interventncular septa and caudal right surface of the right ventricle.
4Main distribution includes the lateral right atrial wall towards the sinoatrial node and sometimes the extension across the coronary groove into the
right longitudinal, sulcus.
5Main distribuhon may include the left atrium, right atrium, right side of the left ventricle, interatrial and interventricular septa on the right side, and
the right caudal portion of the right ventricle.
6Main distribution to the dorsal atrial walls, great vessels, and intermingling of incoming branches which may then pass with major branches to the other
five areas.
Recurrent cardiac nerves
Caudal vagal cardiac nerves
Cranial vagal cardiac nerves
Cranial cervical cardiac nerves
Middle cervical cardiac nerves
Vertebral cardiac nerves
Intermediate cardiac nerves
Cervicothoracic cardiac nerves
Thoracic cardiac nerves
Nerves
TABLE 2
Distribution of cardiac nerves in the Feline
548
JOHN SCOTT McKIBBEN AND ROBERT GETTY
at least to the sixth, seventh, and eighth
cervical spinal nerves, grossly. The ganglia
bilaterally were approximately the same
size (table 1).
Typically two or three cardiac nerves
arose from the caudal portion of the LEFT
cervicothoracic ganglion. A caudodorsal
cervicothoracic cardiac nerue passed caudally along the dorsolateral border of the
left subclavian artery and near this vessel’s
origin joined a left caudoventral cervicothoracic nerve. The LEFT caudoventral cervicothoracic cardiac nerves followed the
caudal limb of the ansa subclavia, then the
left vagus towards the heart. The combined
nerves passed over the left lateral surface
of the aorta and rantified near the caudal
border of the aortic arch. Here left cranial
vagal cardiac nerves and left vertebral
cardiac nerves also joined them. Principal
branches passed caudoventrally, lateral to
the pulmonary artew, and continued between the left auricle and pulmonary veins
to the caudal portion of the coronary groove.
They continued along the course of the circumflex branch of the left coronary artery
to the right side of the left ventricle and
into the right longitudinal sulcus. Branches
Abbreviations
1
2
3c
3d
3e
3f
3g
3h
Ramus communicans
Sympathetic trunk
Third thoracic ganglion
Fourth thoracic ganglion
Fifth thoracic ganglion
Sixth thoracic ganglion
Seventh thoracic ganglion
Eighth thoracic ganglion
3j Ninth thoracic ganglion
4 Cervicothoracic ganglion
5 Ansa subclavia (caudal limb)
5’ Ansa subclavia (cranial limb)
7 Intermediate ganglion
8 Vertebral ganglion
10 Cranial cervical ganglion
11 Vagus nerve
12 Right recurrent laryngeal nerve
12’ Left recurrent laryngeal nerve
13 Thoracic cardiac nerve
14’ Caudodorsal cervicothoracic cardiac nerve
14” Caudoventral cervicothoracic cardiac nerve
16 Vertebral nerve
17 Intermediate cardiac nerve
18’ Caudal vertebral cardiac nerve
20 Cranial cervical nerve
21 Cranial vagal cardiac nerve
21’ Caudal vagal cardiac nerve
22 Recurrent cardiac nerve
24a Eighth cervical spinal nerve
24b Seventh cervical spinal nerve
24c Sixth cervical spinal nerve
24d Fifth cervical spinal nerve
24e Fourth cervical spinal nerve
24f Third cervical spinal nerve
25a First thoracic spinal nerve
25b Second thoracic spinal nerve
25c Third thoracic spinal nerve
25d Fourth thoracic spinal nerve
25e Fifth thoracic spinal nerve
25f Sixth thoracic spinal nerve
25g Seventh thoracic spinal nerve
25h Eighth thoracic spinal nerve
25j Ninth thoracic spinal nerve
26 Vascular nerve
28 Cardiac plexus
Inferior (nodose) ganglion of the
vagus nerve
Aa First rib
Ab Second rib
Ac Third rib
Ad Fourth rib
Ae Fifth rib
Af Sixth rib
Ag Seventh rib
Ah Eighth rib
Aj Ninth rib
B
Longus colli muscle
C Esophagus
D Intercostal artery
D’ Intercostal vein
E Aorta
F Brachiocephalic artery
G Left subclavian artery
G Right subclavian artery
H Costocervical artery
I
Transverse colli artery (dorsal artery)
Supreme intercostal artery (subcostal artery)
J
K Vertebral artery
L Deep cervical artery
M’ Costocervico-vertebral vein
N’ Left common carotid artery
N Right common carotid artery
0 Right vena azygos
P
Cranial vena cava
Q
Caudal vena cava
R
Right atrium
R‘ Right auricle
S’
Left auricle
T Right ventricle
U Left ventricle
W Trachea
X Bronchus
Y Pulmonary artery
Y Pulmonary vein
Z
Lung
AA Ligamentum arteriosum
BB Right coronary artery
B B Descending branch of left coronary artery
BB” Circumflex branch of left coronary artery
CC Great cardiac vein
FF Middle cardiac vein
29
FELINE CARDIAC INNERVATION
Fig. 1
Feline: Left lateral view of the cardiac nerves and related ganglia.
Fig. 2
Feline: Right lateral view of the cardiac nerves and related ganglia.
549
550
JOHN SCOTT McKIBBEN AND ROBERT GETTY
Fig. 3 Feline: Dorsal view of the cardiac innervation. The sympathetic trunks and vagi
are reflected laterally.
passed to the dorsum of the left auricle,
ventrum of the left atrium, caudal and
right walls of the left ventricle, interatrial
and interventricular septa from the right,
and the caudal right portion of the right
ventricle. Other branches of the left caudoventral cervicothoracic cardiac nerves
passed to the aorta, pulmonary artery, left
pulmonary veins and into the cardiac
plexus. Some twigs continued through the
FELINE CARDIAC INNERVATION
cardiac plexus and between the aorta and
pulmonary artery to join the trunk of combined right cardiac nerves. Together these
nerves followed the right and left coronary
arteries from near their origins to their
ramifications on the right ventricle, left
cranial portion of the left ventricle, and the
cranial and ventral portions of the right
and left auricles.
RIGHT ceruicothoracic cardiac nerves
passed with the caudal limb of the ansa
subclavia to its junction with the right
vagus nerve just caudal to the subclavian
artery. Here they joined right vertebral,
recurrent, and caudal vagal cardiac nerves,
passed caudally on the ventral surface of
the trachea, continued between the cranial
vena cava and aorta and entered the cardiac plexus. The main continuation
through the plexus was followed around
the caudal surface of the aorta to the left
side of the heart. On the left side it proceeded cranially around either side of the
pulmonary artery, then along the right and
left coronary arteries. Branches along these
arteries passed to the right ventricular wall,
cranial left portions of the left ventricle, interventricular septum and the cranial and
ventral portions of the right and left auricles. Other right cervicothoracic cardiac
nerves arising from the caudal limb of the
ansa subclavia passed caudally with the
right vagus nerve to the area of the right
apical bronchus. Here, together with caudal
vagal cardiac nerves, they left the vagus
and proceeded between the right branch of
the pulmonary artery and the cranial vena
cava to ramify on the dorsolateral surface
of the right atrium. Their course onto the
right atrium was between the venae cavae
or between the caudal vena cava and left
atrium. Twigs may extend to the area of
the coronary sinus. Occasionally, independent right cervicothoracic cardiac nerves
passed directly from the right cervicothoracic ganglion to the area of the right
apical bronchus. Here they joined caudal
vagal cardiac nerves and passed to the
right atrium. Twigs from right cervicothoracic cardiac nerves also passed to the
cardiac plexus, right pulmonary artery and
veins, and cranial and caudal vena cava.
C . Cervical ganglia and cardiac nerves
An inconstant INTERMEDIATE GANGLION
of variable size (table 1) was noted on the
551
more caudal of the paired left caudal limbs
of the ansa subclavia in three cats. Intermediate cardiac nerves arising from this
ganglion passed with the left caudoventral
cervicothoracic cardiac nerves to the heart.
No homologous ganglion or nerves were
noted grossly on the RIGHT side.
Each VERTEBRAL GANGLION was located
at the cranial ends of each ansa subclavia,
directly craniomedial to the vertebral
artery, and just dorsal to the vagus nerve.
Each was approximately the same size
(table 1 ) .
Two to four vertebral cardiac nerves
arose from the LEFT vertebral ganglion,
joined into one trunk after passing caudally for a few millimeters, and continued
caudally in close apposition to the left
vagus nerve. Near the caudal border of the
aortic arch it joined the other left cardiac
nerves and passed to areas along the circumflex branch of the left coronary artery
on the caudal and right sides of the heart,
as previously described. Nerves from the
left vertebral ganglion may join a nerve
from the cranial cervical ganglion, and
continue between the brachiocephalic and
left subclavian arteries to reach the aorta.
RIGHT vertebral cardiac nerves, generally
three or four in number, joined the other
right cardiac nerves and passed with them
to the heart, as previously described under
the right cervicothoracic cardiac nerves.
No independent MIDDLE CERVICAL GANGLION was noted grossly in the cat.
The CRANIAL CERVICAL GANGLION lay in
close apposition to the nodose ganglion
ventromedial to the tympanic bulla. It measured approximately 8 mm craniocaudal,
3 mm dorsoventral, and 2 mm mediolateral.
No cranial cervical cardiac nerves were
noted; however, on the left side a completely separable nerve arising from the
cranial cervical ganglion, left cranial
laryngeal nerve, and left vagus accompanied the vagosympathetic trunk caudally. It passed ventral to the left subclavian artery and between the left subclavian artery and brachiocephalic trunk and
ramified on the aorta.
D. Vagal cardiac nerues
In addition to the vagal fibers passing in
the previously described nerve, LEFT
cranial vagal cardiac nerves arose from the
552
JOHN SCOTT McKIBBEN AND ROBERT GETTY
intimately interwoven association of the
left vagus with the sympathetic nerves at
the junction of the aorta, pulmonary artery,
and left bronchus. These nerves followed
the sympathetic nerves from this side into
the cardiac plexus, to the aorta and pulmonary artery, to the caudal and right
aspects of the left ventricle, ventrum of the
left atrium, interventricular and interatrial
septa, and caudal portion of the right ventricle. Twigs may indirectly reach the left
longitudinal sulcus and cranial coronary
groove along the coronary arteries. A RIGHT
cranial vagal cardiac nerve passed with
other right cardiac nerves as described previously for the right cervicothoracic cardiac
nerves.
Two or three caudal vagal cardiac nerues
arose from the LEFT vagus nerve about 5
nun caudal to the origin of the left recurrent laryngeal nerve from the vagus and
passed cranioventrally between the pulmonary veins and left auricle into the coronary groove. The left auricle received twigs
as the nerves passed it. They also ramified
along the circumflex branch of the left
coronary artery onto the caudal and right
surfaces of the left ventricle, ventrum of
the left atrium, interatrial and interventricular septa, and caudal wall of the right
ventricle. Fine twigs sometimes also passed
to the cardiac plexus, the left longitudinal
sulcus, and along the right coronary artery.
From the intimate association of the right
vagus with the right sympathetic nerves, as
the caudal limb of the ansa subclavia approximates the vagus, RIGHT caudal vagal
cardiac nerves combined with sympathetic
and right recurrent cardiac nerves and
passed caudoventrally, ventral to the trachea. Their distribution included the right
ventricle, left and cranial portions of the
left Ventricle, and the cranial and ventral
portions of the auricles. Two or three additional caudal vagal cardiac nerves arose
These accompanied the right cervicothoracic cardiac nerves to the dorsolateral portion of the right atrium, the cardiac plexus,
right pulmonary vessels, venae cavae and
sometimes extended into the coronary
groove in the area of the coronary sinus.
heart grossly. Some ramified, however, on
the caudal border of the aorta. One or two
fine RIGHT recurrent cardiac nerves joined
the sympathetic and vagal cardiac nerve
trunk which originated near the caudal
limb of the ansa subclavia. They passed
together, as previously described, to the
right ventricle, left caudal portion of the
left ventricle, and the cranial and ventral
portions of the auricles.
DISCUSSION
In the present morphologic investigation
thoracic cardiac nerves were found to arise
from the sympathetic trunk between the
cervicothoracic ganglia and fourth or
fifth thoracic ganglia on the right and left
sides, respectively. Perman ('24) and investigators previous to him, did not report
thoracic cardiac nerves in the cat. Anufriew ('28) noted their presence as far
caudal as the second thoracic ganglion only
on the left side. Saccomanno ('43), supporting gross findings with histologic observations, followed them bilaterally from
the upper five or six thoracic sympathetic
ganglia to the cardiac plexus. Thoracic
cardiac nerves are variable in number and
origin between specimens.
Cervicothoracic cardiac nerves have
been traced to the cardiac plexus from each
side by Saccornanno ('43). Perman ('24)
indicated that they passed to the atria,
dorsal walls of both ventricles, and the
lateral wall of the left ventricle from the
left side. In agreement with Anufsiew ('28),
the present authors found that left cervicothoracic cardiac nerves passed primarily to
the dorsum of the left auricle, ventrum of
the left atrium, caudal and right walls of
the left ventricle, interatrial and interventricular septa from the right side, and the
caudal right portion of the right ventricle.
In addition, the present investigators found
branches which continued through the
cardiac plexus to join the combined trunk
of right heart nerves. Both Perman ('24)
and Anufriew ('28) found right cervicothoracic cardiac nerves passing to the ventral portion of the right ventricle and along
the left longitudinal sulcus to both ventricles. In addition, Anufriew ('28) noted
E. Recurrent cardiac nerves
branches to the right auricles and atrium.
Twigs arising from the LEFT recurrent The findings of the present authors are in
laryngeal nerves were not followed to the agreement with Anufriew ('28).
FELINE CARDIAC INNERVATION
The inconstant intermediate ganglion
and intermediate cardiac nerves in the cat
were not reported previous to the present
investigation. Their prominence varied
considerably between specimens and they
were similarly located only in one other
species, the porcine.
In accordance with Wrete ('59) the
term intermediate ganglion is reserved
for small inconstant ganglia situated in
internodal rami between constant ganglia,
as well as in communicating rami or in the
main trunk or roots of spinal nerves.
Though somewhat less than in the
canine, the vertebral cardiac nerves contribute a large portion of the sympathetic
cardiac innervation in the feline. Mannu
('14) and Saccomanno ('43) noted cardiac
nerves from the vertebral ganglia but followed them only to the cardiac plexus.
Perman ('24) noted their distribution from
each side to the cranial portion of the right
ventricle. Anufriew ('28) did not recognize these nerves. The present authors
found that vertebral cardiac nerves passed
to each of the major areas of distribution
(table 2).
Cervical cardiac nerves were not noted
from the cranial cervical ganglion, nor was
a middle cervical ganglion noted grossly.
Vagal cardiac nerves, in agreement with
Anufriew ('28), were followed to each of
the major areas of distribution (table 2 ) .
Both the atria and ventricles received fibers.
Left recurrent cardiac nerves were not observed, though submacroscopic communications are suspected. Right recurrent
cardiac nerves joined and were distributed
with other right cardiac nerves.
Though the origin, course, and distribution of cardiac nerves of the feline re-
553
semble those of the canine, generally, they
combined on each side in the cat resulting
in large trunks to specific areas. However,
through communication with the cardiac
plexus several areas could be supplied by
a single trunk.
ACKNOWLEDGMENT
The appreciation of the authors is extended to Dr. D. J. Hillman for the photography.
LITERATURE CITED
Anufriew, W. N. 1928 Die Herznerven des
Katze. Ztschr. f. Anat. u Entwg., 86: 639-654.
Bernhardt, E. 1868 Anatomische und physiologische Untersuchungen uber den Nerve depressor bei der Katze. Dissertation Dorpat.
Original not available; cited in Anufriew, W. N.
1928 Die Herznerven des Katze. Ztschr. f.
Anat. u Entwg., 86: 639-654.
Boehm, R. 1875 Untersuchungen uber den
Nervus accelerator cordis der Katze. Arch. f.
Exp. Path. u Pharm., 4 : 255-279.
Kazem Beck, A. 1888 Beitrag zur Innervation
des Herzens Arch. f. Anat. u Phys., 12: 325349.
Mannu, A. 1914 Ricerche anatomocomperative
sul simpatico cervicale nei mammiferi. Intern.
Monatsschr. f. Anat. u Physiol., 30: 49-168.
McKibben, J., and R. Getty 1968 A comparative morphologic study of the cardiac innervation in domestic animals. I. The canine. Am.
J. Anat., 122: 533-544.
Nonidez, J. F. 1939 Studies on the innervation of the heart. I. Distribution of the cardiac
nerves, with special reference to the identification of the sympathetic and parasympathetic
postganglionics. Am. J. Anat., 65: 361-401.
Perman, E. 1924 Anatomische Untersuchung
uber die Herznerven bei den hoheren Saugetieren und bei Menschen. Ztschr. f. Anat. u
Entwg., 71: 382-457.
Saccomanno, G. 1943 The components of the
upper thoracic sympathetic nerves. J. Comp.
Neur., 79: 355-379.
Wrete, M. 1959 The anatomy of the sympathetic trunks in man. J. Anat., 93: 448-459.
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