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Functional anatomy of the cardiac nerves in the baboon.

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Functional Anatomy of the Cardiac
Nerves in the Baboon'
WALTER C. RANDALL, J. ANDREW ARMOUR, DAVID C. RANDALL
AND ORVILLE A. SMITH
Departments of Physiology, Loyola University, Chicago, and t h e
University of Washington, Seattle, and t h e Regional Primate
Research Center, University of W a s h i n g t o n , Seattle
ABSTRACT
In 17 anesthetized baboons, the autonomic innervation of the
heart was carefully exposed and electrically stimulated to determine the course
of fibers having direct inotropic and/or chronotropic actions. The superior cervical and nodose ganglia are intimately associated by means of short but large
interconnections, and the sympathetic and parasympathetic trunks descend with
the carotid artery in a common epineural sheath. The middle cervical ganglion
is invariably well defined and completely separated from the vagus trunk in the
upper portion of the thoracic cage. Direct nervous connections between the sympathetic and vagal trunks are frequent at all levels within the thorax. Both systems also send small nerves into the phrenic and recurrent laryngeal nerves.
Separate inferior cervical and first thoracic ganglia were not found, but rather,
a large and well defined stellate ganglion extending across the heads of the first
and second ribs. The stellates are connected to the middle cervical ganglia by
means of both dorsal and ventral ansae subclavia of varying size. Although fine
nerves arising from the upper thoracic trunk were located, they appeared to have
no direct inotropic or chronotropic actions. The major sympathetic and parasympathetic nerves converge upon richly interconnected dorsal and ventral cardiopulmonary plexuses and several minor (superior vena cava, left atrial, pulmonary veins) plexuses. Both ipsilateral and contralateral control of cardiac
function is possible through these pathways. The baboon cardiac innervation
thus appears to resemble that of man in some respects and the dog in others.
The nerve supply to the canine heart has
been investigated in considerable detail including emphasis upon both anatomic and
functional systems. Similarly, the cardiac
innervation in man is well described anatomically, but due to obvious difficulties
in carrying out experimental procedures in
man, relatively few functional responses
to nerve stimulation have been reported.
Recent interest in the question of cardiac
reinnervation following surgical transplantation reiterates the importance of
more precise knowledge of this system.
Direct carry-over of information from the
experimental animal (dog, cat, rabbit) to
primates may not be permissable, and
therefore, it was decided to experimentally
pursue several pertinent questions concerning the innervation of the heart in
nonhuman primates.
ANAT. REC.,170: 183-198.
Diligent search of the literature failed to
reveal significant information on the gross
innervation of the nonhuman primate
heart. A description by Kuntz ('33) in the
autonomic nervous system of the Rhesus
monkey proved to be grossly inadequate.
Sketches by Perman ('24) are so diagrammatic as to be of little use. Regiele ('26)
described in considerable detail his dissections in a single baboon with sketchy
confirmation from a second specimen.
These workers did not, of course, include
functional data in their descriptions. Thus,
it became apparent that while a few important physiological, surgical and behavioral studies have been performed in
Received June 24, '70. Accepted Oct. 14, '70.
1 Supported by NIH grant HE 08682 to Loyola University and grant FR 00166 to the Regional Primate
Research Center, Seattle.
183
184
W. RANDALL, J. ARMOUR, D. RANDALL AND 0. SMITH
this group of animals, few if any structurefunction relationships have been reported.
A very real need exists for both anatomical
description and functional testing of the
autonomic cardiac nerves in the nonhuman primate, and consequently the
present experiments were undertaken on
the baboon.
METHODS
Acute experiments were carried out in
seventeen open-chest baboons (Papio anubis and Papio cynocephalus) anesthetized
with Serynlan (0.2 to 1.0 mg/kg) and
chloralose (20 to 60 mg/kg) in propylene
glycol. Modified Walton-Brodie strain gauge
arches were stitched to the epicardial surfaces of all four cardiac chambers, frequently with two gauges on both left and
right ventricles. These gauges permit essentially isometric recording of contractile
force from an approximately 1 cm segment
of myocardium. Artificial respiration was
supplied by means of a Bird Mark 7
respirator. Arterial blood pressure (and/or
in traventricular pressure) was recorded by
Statham P23Db pressure transducers with
all recordings on a model R Beckman
Dynograph.
All visible nerves were carefully dissected in the thoracic region from the clavicle to the level of approximately T6, including, of course, the cardiac nerves.
Each nerve on both right and left sides was
stimulated by means of bipolar electrodes
and either a Grass model 5 square wave
voltage generator or a Nuclear-Chicago
model 7151 constant current stimulator.
When using the voltage generator the stimulating voltages were monitored on a cathode ray oscilloscope and maintained at the
stated level throughout the period of stimulation. Immediately following stimulation,
an identifying ligature was loosely looped
around the nerve at the point of stimulation for later anatomical identification. In
addition, the vagosympathetic trunk in the
neck was carefully dissected free and the
sympathetic trunk separated from the
vagus, so that each trunk could be isolated
and electrically stimulated. Thus, electrodes were successively applied to the
cervical vagosympathetic trunk as well as
to its individual components, to the thoracic
vagus, to each of the small nerves taking
origin from the middle cervical ganglion,
dorsal and ventral ansae, caudal pole of
the stellate ganglion, and to the interganglionic segments from T3 through T6, the
latter both before and after transection of
the trunk above and below each ganglion.
RESULTS
The efferent innervation of the baboon
heart consists of fibers coursing in the
vagus and in the cervical-thoracic sympathetic nerves. Contrary to conventional
concepts, these divisions of the autonomic
nervous system are neither anatomically
nor functionally isolated from each other,
since direct and frequently profuse interconnections occur at all levels including
the superior cervical, middle cervical and
stellate ganglia.
Figures 1 and 2 present detailed descriptions of the typical anatomic distribution
of autonomic nerves to the baboon heart.
Variable interconnections exist between
right and left sides including branchings
from both sympathetic and vagus trunks.
There exists a concerted flow of nerves
from the lateral position of the stellate and
middle cervical ganglia, medially and caudally, to enter the large plexuses situated
over the tracheal bifurcation, the pulmonary artery, and aortic arch. These plexuses
are intimately interconnected and are extended distally to both atria, large central
veins and arteries to provide innervation
for both ventricles. Thus, nearly every portion of the heart is provided with innervation from both right and left sympathetic
and parasympathetic trunks. In addition,
there generally exist major pathways directly from the right sympathetics to the superior vena cava and right atrium as well
as from the left middle cervical ganglion
(and sometimes the stellate) to the posterior surface of the left atrium and
ventricle.
The cervical vagosympathetic trunks
The superior cervical ganglion is situated
medial to the nodose ganglion on either
side at the level of C2-C3. The two ganglia
are tightly interconnected by means of a
varying number of short but large nerves,
and receive connecting rami from, or
branching to, the pharynx, esophagus,
laryngeal and hypoglossal nerves, the
CARDIAC NERVES IN THE BABOON
185
Fig. 1 Ventral view of the primary cardiac nerves on the left side, baboon 8. Dashed lines indicate the nerves course dorsal to the overlying structure.
plexuses on the external and common caro- clature in existing descriptions of this systid artery, and the upper three or four tem in higher mammals including man,
cervical nerves. The large cervical sym- we have elected to employ those names
pathetic trunk enclosed within its sheath, most commonly accepted for the primary
extends from the caudal pole of the su- structures (stellate, middle cervical ganperior cervical ganglion and joins with the glion, vagus, phrenic, etc.) and appropriate
vagus approximately 1.5 cm distal to the anatomically descriptive names for the
caudal pole of the nodose ganglion. Thus, nerves themselves. In this way it is hoped
while the cervical sympathetic and vagus that we may convey a three dimensional
are each invested within their own sheaths, picture of the nervous projections onto the
both are wrapped within a common sheath multidimensional surfaces of the heart.
as they descend caudally with the carotid Our nomenclature thus substitutes the
artery. They are readily separated at any term dorsal cardiopulmonary plexus for the
level between the superior and middle conventional “pretracheal” or “deep” cardiac plexus and the term ventral cardiocervical ganglia.
Figure 1 illustrates the origin of cardiac pulmonary plexus for “aortic” or “supernerves on the left while figure 2 shows a ficial’’ plexus. Our objective is to emphasize
comparable display on the right, both ac- the facts, recognized by Mizeres (’63) and
curately reflecting the anatomic origin and McKibben and Getty (’69), that there is
course of the major cardiac nerves. In view no real separation between deep and superof the remarkable differences in nomen- ficial divisions nor separation from the pul-
186
W. RANDALL, J. ARMOUR, D . RANDALL A N D 0. SMITH
Fig. 2
Lateral view of the primary cardiac nerves on the right, baboon 8.
monary plexus. Rather, there is demonstrable input to a common plexus from
both right and left sides and from both
sympathetic and parasympathetic divisions
with rich interconnections at every level.
Further, it is important to recognize that
visual separation of the cardiac and pulmonary innervations is impossible at the
plexus level, and interruptions here invoke
alterations in both cardiac and pulmonary
functions. Finally, it should be noted that
many large nerve trunks maintain continuity through the plexus with direct projections onto different surfaces of the
heart including both atrial and coronary
plexuses.
Figures 3 and 4 illustrate the responses
to electrical stimulation of the cervical
vagus and sympathetic trunks, as well as
the combined vagosympathetic complex,
in a single animal. In figure 3A, the isolated sympathetic portion of the right trunk
was stimulated with positive inotropic and
chronotropic alterations developing in all
test segments. Heart rate accelerated from
control levels of 162/minute to a maximum of 198/minute while arterial blood
pressure increased from 65/46 to 80/50
mm Hg. Augmentation in contractile force
was most pronounced on the right heart,
particularly in the right atrium (RA) and
right ventricular sinus (RVS) which encompasses the inflow tract of the right
ventricle. Augmentation was not prominent on the left heart but was discernible
on both apex (LVA) and base (LVB). Alterations in rate of increase in contractile
force were also indicated (dF/dt) as measured from the ascending slopes of the
fast traces in each myocardial segment.
Panel B shows bradycardia (HR 162 to
84/minute) and decreased arterial blood
pressure (65/40 to 40/20 mm Hg), together with suppression in contractile force
and dF/dt, on some segments during
stimulation of the vagal portion of the
H
10 scc
H
200mscc
RT. CERV. VAGUS
B
-
RT. VAGO. SYMP.
C
Fig. 3 Responses to electrical stimulation (10 cps, 5.0 msec, 4.0 v ) of the caudal pole of the
superior cervical ganglion (panel A ) , caudal pole of nodose ganglion (panel B ) , and of the combined right vagosympathetic trunk 1.5 cm distal to the junction of the cervical sympathetic and vagal
trunks (panel C ) , baboon 16. The period of stimulation is indicated by the signal marker i n each
panel.
mmHg
BP&wwwdUuL-0
RT. CERV. SYMP.
A
MAR19170
-
4
188
W. RANDALL, J ARMOUR, D. RANDALL AND 0. SMITH
.
0
h
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K
a
I
E
CARDIAC NERVES IN THE BABOON
vagosympathetic trunk. Right atrial contractile force showed the greatest amount
of inhibition with relatively little suppression in force on RVS and LVA. Note the
progressive recovery of heart rate and contractile force following cessation of stimulation, unaccompanied by post-stimulation
tachycardia or overshoot in contractile
force. Panel C presents responses to identical electrical stimulation of the combined
vagosympathetic trunk 1 cm distal to the
point of stimulation of each of the components illustrated in panels A and B. Although bradycardia occurred (162 to 102/
minute) it was of lesser magnitude than
induced during similar stimulation of the
vagus alone. Whereas depression in contractile force was less in the right atrium,
i t was essentially comparable to that in
panel B in the left atrium. Contractile
force was inhibited only on the left ventricular base, whereas that on all other
ventricular test segments was augmented.
Careful scrutiny of the ventricular records
reveals almost exact algebraic summation
of responses to separate stimulation of the
sympathetic (3A) and parasympathetic
(3B) trunks. Mean arterial pressure showed
little or no change although pulse pressures were distinctly increased. Post-stimulation “rebound in contractile force was
prominent in the atrial traces and postvagal stimulation tachycardia ( 192/minUte) was evident in the recovery traces
immediately following cessation of stimulation.
Figure 4 shows responses to separate
electrical stimulation of the left cervical
vagosympathetic trunk in the same baboon
as illustrated in figure 3. During excitation
of the sympathetic portion of the trunk
(3A), acceleration in heart rate (168 to
180/minute), increased arterial blood pressure (65/45 to 75/50), and augmentation
in contractile force occurred. The latter
characterized all myocardial test segments
and was accompanied by increased dF/dt.
Excitation of the vagal component (panel
B) induced cardiac slowing (162 to 120/
minute) and decreased contractile force.
The latter was most prominent in the
atrial traces but was distinctly apparent
in all chambers. Recovery in both heart
rate and contractile force was gradual and
did not show postvagal tachycardia or re-
189
bound. Stimulation of the combined vagosympathetic trunk (panel C ) elicited
changes in cardiac dynamics showing characteristics of both of the previous procedures (A and B). The induced bradycardia
was less intense (164 to 150/minute),
the decline in arterial blood pressure
was minimal, and inhibition in contractile
force was confined primarily to the right
atrium where i t was much less intense. Recordings from several ventricular segments
actually showed increased contractile force.
There appeared a modest postvagal tachycardia (to 175/minute) and clear “overshoot” in contractile force of the atrial
segments.
Comparison of the indivdual myocardial
segment responses in figures 3 and 4 reveals qualitative as well as quantitative
difference in responses. Note, for example,
the greater magnitude of right atrial response during excitation of the right vagosympathetic components. While the right
stimulations excited relatively marked augmentation in contractile force of both right
ventricular segments, left side stimulation
elicited only minor changes. The primary
distribution of augmentor fibers to the left
atrium is by way of the left sympathetics.
Thus, in spite of great intermingling of
nerves from right and left, there is evidence for localized distribution of both components of the autonomic innervation of
the primate heart.
Electrical excitation of the vagus trunk
in the thorax as compared with vagosympathetic stimulation in the neck further
revealed a different composition of the
nerves in these two locations. Figure 5 illustrates such stimulations before and after
atropine. Panels A and B demonstrate typical responses to electrical excitation of the
right thoracic (A) and cervical (B) vagosympathetic trunks, while panels C and D
represent comparable stimulations on the
left. In each instance the thoracic vagus
exerted greater negative inotropic and
chronotropic influences than did the cervical levels of the vagosympathetic trunks.
The per cent changes in arterial blood
pressures were correspondingly less during
stimulation of the cervical trunks.
After atropine, identical stimulation
elicited slight to moderate positive inotropic
and chronotropic responses, indicating the
W. RANDALL, J. ARMOUR, D. RANDALL A N D 0. SMITH
In
>
U
CARDIAC NERVES IN THE BABOON
191
often be traced across to the large nerves
and the middle cervical ganglion on the
opposite side (figs. 1, 2, 6).
Distinct and sometimes large nerves
connect directly between the ventral ansa
or the stellate ganglion and the vagus nerve
(stellate vagal nerve). These were often in
addition to smaller connections on the
right between the inferior loop of the recurrent nerve and the ventral ansa. Rich
intermingling of vagus and sympathetic
nerves occurred caudal to the middle cervical ganglion. The cardiopulmonary plexus
arises from multiple branches from both
sympathetic and parasympathetic trunks
(fig. 6). From two to five nerves coursing
Middle cervical g a n g l i m
toward the heart from the left middle
The middle cervical ganglion is remark- cervical and stellate ganglia send major
ably variable in size and shape, occasion- projections to the region of the tracheal
ally consisting of several small ganglionic bifurcation, the root of the pulmonary
swellings connected in series. The superior artery, and to the concavity of the aortic
poles of the ganglion receives several small arch. The left recurrent nerve arises as a
nerves, described by Riegele as coming major branch of the vagus at the level of
from the third through the sixth cervical the aorta which it encircles, its branches
nerves. There are also a variable number intermingling with sympathetic nerves
of small nerves which interconnect with from the middle cervical ganglion, and
the recurrent, the phrenic and the vagus courses rostrally. Many nerves pass from
nerves. In many instances fine nerves may the aortic arch to the ventral surfaces of
be traced from the ganglion in both direc- the pulmonary artery and along its right
tions along the subclavian artery. Com- and left primary divisions, as well as to the
pletely encircling the subclavian artery the left atrium and pulmonary veins. Extendorsal and ventral ansae interconnect the sions of this plexus invest the coronary
middle cervical and the stellate ganglia. In arteries to innervate both right and left
some animals the ventral ansa is larger ventricles.
than the dorsal but in a majority, the dorsal
A majority of the larger nerves from the
ansa is more massive. Small nerves branch right sympathetics and vagus converge on
off both ansae and pass either superiorly the region between the aorta and pulto join with rami of the cervical nerves or monary artery and contribute to the dense
enter plexuses around the subclavian and plexus dorsal to the aortic arch and overinnominant arteries. Fiber connections can lying the bifurcation of the trachea. It is
Fig. 5 Responses to electrical stimulation (10 comparable to the pretracheal or deep cardiac plexus described in the dog and man.
cps, 2 msec, 0.3 m a ) of the vagosympathetic
It also receives multiple branches from the
nerves in the cervical and thoracic regions before
(upper) and after (lower) atropine (1.0 mg/kg).
vagosympathetic system on the left, and
Onset and duration of stimulation is indicated
is richly interconnected with the plexus
by signal marker at top of channel 1. Strain
situated in the arch of the aorta. There
gauge arches were applied to the right atrium
( R A ) , right ventricular conus (RVC), right ven- are prominent extensions to the right
tricular sinus (RVS), and left ventricular base
atrium, superior vena cava, right pulmon(LVB). Systemic arterial blood pressure is shown
ary artery and veins. In order to preserve
in channel 5 . All records were made following
appropriate dorso-ventral relationships
bilateral cervical vagotomy and decentralization
of the upper thoracic sympathetic trunk. Stimula- without obfuscation from the plethora of
tions were applied to the right thoracic vagus
existing interconnecting nerves, only a few
( A and E ) , peripheral end of the right cervical
of
the major contributions from the right
vagosympathetic trunk (B and F ) , left thoracic
vagus (C and G), and left cervical vagosympa- and left cardiac nerves are depicted in
figure 6 .
thetic trunk (D and H).
presence of sympathetic fibers in these
nervous structures conventionally thought
to be exclusively parasympathetic. The increases in heart rate varied from 20 beats/
minute in E, 15/minute in F and G , and
lO/minute in H. With exception of the
right thoracic vagus (panel E), all responses were characterized by augmentation in contractile force on both right and
left atrial and ventricular surfaces. Thus,
the presence of both sympathetic and parasympathetic fibers in the vagosympathetic
trunks, both superior and inferior to the
middle cervical ganglion is clearly indicated.
192
W. RANDALL, J. ARMOUR, D. RANDALL A N D 0. SMITH
Fig. 6 Sketch of the cardiopulmonary plexus from left lateral view. In order to reveal important
dorso-ventral relationships of the plexus, as well as the rich interconnections between these levels,
only a portion of the major cardiac nerves descending from the right and left vagosympathetics are
shown.
Figure 7 illustrates the considerable variability in anatomical structure of the middle cervical ganglion and its ansal connections with the stellate. In none of the
seventeen specimens dissected could separate inferior cervical and first thoracic ganglia be differentiated, all showing distinct
and large cone-shaped stellate ganglia on
both sides. In some animals the ventral
ansa was large and represented the primary connection between the stellate and
middle cervical ganglion (fig. 1). In many
animals the dorsal ansa was the more massive and often fused directly with the middle cervical ganglion (fig. 7). The ventral
ansa was occasionally very tiny and gave
rise to no subsidiary nerves. In a few instances, distinct ganglionic swellings were
small or absent and the ansae themselves
were enlarged and gave rise to cardiac
nerves.
On the left, the vagus descended medial
to the middle cervical ganglion and in most
specimens made direct neural interconnection with it. On the right, the vagus
generally crossed directly over the subclavian artery at the level of the junction
between the ansa subclavia and the middle
cervical ganglion. Here again numerous
discrete, small nerves connected the sympathetic and parasympathetic systems. In
no instance was the middle cervical ganglion wrapped within a common epineurium with the vagus as is generally true
in the dog. The vagus continued distally
and gave rise to the recurrent nerve which
in turn contributed large branches to the
cardiac plexuses.
The middle cervical ganglion on the right
was sometimes discrete and globular (fig.
2), but in other animals consisted of a
series of small ganglionic swellings fused
together and gave rise to nerves which
passed both superiorly and inferiorly along
the subclavian and innominate arteries.
Fewer nerves were sent directly to the cardiac plexus than from the left, but rich
communication with the vagus and recurrent nerves provide sympathetic pathways
to the heart. Riegele noted numerous small
193
CARDIAC NERVES IN THE BABOON
RECURRENT
MIDDLE
CERVKP
s1'ELLATE ' 8 .
RtGHT SIDE
LLATE
LEFT SIDE
RECURRENT
Fig. 7 Illustrating anatomic variations in form and structure of the stellate and middle
cervical ganglia in the baboon (all different from figs. 1, 2). Note differences in ansal connections, the origins of nerves, and the variable patterns of interconnection between sympathetic and parasympathetics.
connections from this ganglion (or its
ansae) with the C3-C7 nerves. Electrical
stimulation of the stellate ganglion or the
ansa subclavia often caused marked bradycardia and arrhythmia accompanied by
augmentation in cardiac contractile force.
Although such arrhythmias are sometimes
encountered during stimulation of the left
stellate in the dog, they are less common
during excitation of the right sympathetics
in this species. Another functional variation in responses to stellate stimulation in
the two species (baboon and dog) is related to heart rate. In the dog, the right
sympathetics generally (not invariably)
cause greater acceleration in heart rate
with lesser influence on systemic arterial
pressure. Stimulation of the left stellate
frequently exerts little or no influence on
heart rate but elicits large changes in ventricular pressure and systemic arterial
pressure. Such dichotomy in response was
less evident in the baboon, and both heart
rate and contractile force changes were
generally associated with both right and
left sympathetics.
The thoracic vagus
The left vagus often gives rise to one
or two large cardiac nerves just superior
to the middle cervical ganglion. These may
have rich interconnections with the posterior ansa, the middle cervical ganglion,
and with the cardiac nerves originating
from the ganglion. There are also branches
coursing to the subclavian and left common
194
W. RANDALL, J. ARMOUR, D. RANDALL A N D 0. SMITH
carotid arteries and to the trachea. Inferiorly these nerves divide and send multiple branches into the cardiopulmonary
plexus. There are also numerous fine neural connections with the phrenic nerve, the
pericardium, and pulmonary veins.
The right vagus is anatomically very
close to the middle cervical ganglion, and
gives off a large recurrent nerve which
loops around the subclavian artery and ascends parallel to the cervical vagosympathetic trunk. At its point of origin from the
vagus it gives rise to a large independent
nerve which quickly divides and repeatedly
interconnects with both sympathetic and
vagal components along its course to
the cardiopulmonary plexus. This nerve
we have called the recurrent cardiac nerve
(figs. 2, 7). Its electrical stimulation elicited
either or both sympathetic and parasympathetic effects, the responses being functionally differentiated by the use of atropine
to block the cholinergic responses. As the
right thoracic vagus descends it crosses the
vena cava, passes dorsally along the pericardium over the right atrium and gives
off many branches to it and to the main
branches of the pulmonary arteries and
veins.
Stellate and upper thoracic
sympathetic ganglia
The stellate ganglion was consistently
found along the anterior aspect and extending from the head of the first to the
second rib. It measured 1.5 to 2 cm in
length, 5 to 7 mm in width at its superior
end and tapering to 1 or 2 mm at its caudal
pole. It typically gave rise to rami to the
sixth, seventh, and eighth cervical nerves
and to the first and second thoracic nerves
with those from T3 sometimes entering at
its caudal pole. Sender rami sometimes
passed from the rostral pole to join the
subclavian and vertebral arterial plexuses.
In only a few specimens did a distinct
nerve arise from the medial aspect of the
rostral pole to course directly to the cardiac
plexus (inferior or stellate cardiac nerve).
Caudally, the thoracic sympathetic trunk
consisted of segmental ganglia, each connected with its associated intercostal nerve
by both white and gray rami. From the
medial side of the ganglia (and frequently
from the interganglionic segment) arose
multiple small fibers passing to the thoracic
viscera, including pulmonary veins, pericardium and cardiopulmonary plexus.
Figures 8 and 9 illustrate an investigation of the functional role of small nerve
fibers which may be traced from the upper
thoracic sympathetic trunk directly toward
the heart. Panel 8A shows slight augmentation in force of contraction on the ventricular surfaces, together with a marked elevation in arterial blood pressure elicited by
electrical stimulation of the left sympathetic trunk at the interganglionic segment
between T5 and T6. Right atrial contractile force was simultaneously suppressed
with partial A-V block. The left thoracic
trunk was then surgically sectioned immediately above the T5 ganglion and stimulation repeated at the T5-T6 segment with
marked attenuation in response (8B). The
thoracic trunk was next transected below
the T6 ganglion, followed by stimulation
at T5-T6 with abolition of all cardiac response (8C). We conclude from these results that some fibers destined for the
heart ascended in the sympathetic trunk at
this level, but that a minor fraction of the
response in panel A was dependent upon
electrical excitation of the splanchnic innervation. These were obliterated by transection at T6. The complete absence of response during stimulation of the isolated
ganglion at T5 argues strongly against direct transthoracic pathways from this ganglion having any inotropic, dromotropic,
or chronotropic action on the heart. The
suppression in atrial contractile force was
presumably related to the operation of
baroreceptor reflexes. Stimulation at the
T3-T4 segment next revealed an excellent
cardiac response with participation of all
test segments and elevation in arterial
blood pressure (8D). Transection of the
trunk at T3 followed by repeated stimulation of the isolated T4 ganglion again failed
to induce any appreciable cardiac response
(8E). The electrodes were then placed on
the caudal pole of the left stellate ganglion at the vertebral level of T2 with resultant augmented contractile force (8F)
and elevation in blood pressure, again with
atrial depression and A-V block. A somewhat lesser response was elicited by stimulation of the ventral ansa ( G ) , as compared
195
CARDIAC NERVES IN THE BABOON
A
B
C
D
RVS
Fig. 8 Responses to electrical stimulation (10 cps, 2 msec, 0.3 ma) at the interganglionic segments of the upper thoracic sympathetic trunk on the left, baboon 4. Panel A stimulation interganglionic segment T5-T6; panel B, repeat stimulation at T5-T6 after surgical section above T5
ganglion; panel C, repeat stimulation at T5-T6 after section below T6 ganglion; panel D, stimulation
at T3-T4 segment; panel E, repeat stimulation after section at T3; panel F, stimulation caudal pole
left stellate ganglion; panel G, stimulation ventral ansa; H, stimulation dorsal ansa.
with that elicited from excitation of the
dorsal ansa (H).
The virtual absence of cardiomotor response to electrical stimulation of the right
thoracic sympathetic trunk at the T5-T6
interganglionic segment in the same animal (shown in fig. 8) demonstrates a distinct variation in level of outflow with respect to fibers ascending to the heart as well
as those descending to the splanchnic system (fig. 9A). Placement of the electrodes
at the T3-T4 segment however, induced excellent overall cardiac response (9B) which
was abolished after transection of the
trunk at T3 (9C). Again, there was little
or no visible evidence for direct cardiomotor influences of nerves arising from this
portion of the thoracic trunk. Excitation of
196
W. RANDALL, J. ARMOUR, D. RANDALL AND 0. SMITH
I-
a
RVS
II
LVB
Lo
Fig. 9 Responses to electrical stimulation ( a s in fig. 8 ) upper thoracic sympathetic trunk on the
right, baboon 4. Panel A, stimulation interganglionic segment T5-T6; panel B, stimulation a t T3-T4
segment; panel C, stimulation T3-T4 after surgical section a t T3; panel D, stimulation ventral
ansa; panel E, stimulation dorsal ansa; panel F, stimulation caudal pole right stellate ganglion.
the ventral (9D) and dorsal (9E) ansae
elicited positive inotropic and chronotropic
responses. Stimulation of the caudal pole
of the right stellate ganglion induced similar alterations in heart rate as well as in
contractile force (9F).
DISCUSSION
As Mizeres ( ' 6 3 ) found in describing the
cardiac nerves in man, no constant pattern
of nerve distribution from the superior,
middle and stellate ganglia was observed
in the baboon. Except for the main cervical
sympathetic trunk enveloped with the vagus within the carotid sheath, no separate
cardiac nerve descends from the superior
cervical ganglion. Interconnections between the sympathetic and parasympathetic trunks exist between the nodose and
superior cervical ganglia, at the level of
CARDIAC NERVES IN THE BABOON
197
the middle cervical ganglia, and profusely tility is invariably suppressed during vagal
at all levels distally into the cardiopul- stimulation. However, in panels B and C
monary plexus themselves. Thus, anatomi- of figures 3 and 4, atrial contractile force
cal substrate within the cervical vagosym- was dramatically reduced while ventricular
pathetic trunk for both positive and contractile force either increased or denegative inotropic and chronotropic regu- creased, depending upon the predomilation of cardiac activity is provided. There- nance of sympathetic or parasympathetic
fore, careful separation and testing of in- fibers. Predominance of right sided reguladividual nerve pathways must be assured tion of heart rate and left sided control
before either “purely” sympathetic or para- of contractile force as observed in the dog
sympathetic control may be assumed.
by Randall and Rohse (’56) was not promiThe convenient tendency to interpret
nent
in the baboon. Connections between
results of cervical vagosympathetic stimuright
and left thoracic cardiac rami would
lation only in terms of parasympathetic resuggest
a significant difference from husponses has been discussed elsewhere by
Randall, Pace, Wechsler and Kim (’69). man anatomy if Mizeres’ (’63) observaThe interpretation of “postvagal tachy- tions are correct but illustrate similarity
cardia” as resulting from excitation of with human anatomy if one accepts the
cholinergic parasympathetic fibers leading anatomical descriptions of Ellison and
to liberation of catecholamines by Copen, Williams (’69).
In none of the animals was there disCirillo and Vassale (’68), as well as the
cholinergic-link hypothesis of Burn and tinction between inferior cervical and first
Rand (’59) appear to be untenable. Figures thoracic ganglion. That is, a clearly de3 and 4 reveal the sharp, differential re- fined, large stellate ganglion was invarisponses to separate electrical excitation of ably located at the head of the first and
both sympathetic and parasympathetic second ribs. This is in contrast to the obcomponents of the vagosympathetic trunk. servation in man that a fusion of inferior
Eserine fails to unmask any adrenergic re- cervical and first thoracic ganglia occurs
sponse to “purely” vagus stimulation. Post- in 37.7% (Becker and Grunt, ’57), 75vagal tachycardia may result from elec- 80% (Mitchell, ’53) or 88% (Ellison and
trical stimulation of the combined cervical Williams, ’69) of cases. In this respect,
vagosympathetic trunk, but does not follow then, the baboon more closely resembles
excitation of the parasympathetic com- the dog. Distinct ventral and dorsal ansae
ponent alone. Thus in studies involving subclavia were found on both sides of all
autonomic innervation of the heart, sym- animals, connecting the stellate and midpathetic responses must be separated, both dle cervical ganglia. Considerable varianatomically and functionally, from para- ability was found, however, in their relasympathetic responses before consideration tive size. Corresponding variations in
of the release of norepinephrine by acetyl- functional control were exerted by the two
choline is warranted. A straight-forward ansae, the larger structure generally elicitinterpretation of direct responses to cholin- ing the more profound cardiac responses
ergic or adrenergic nerves satisfies all ex- when electrically stimulated. The upper
perimental results in both the dog (Ran- four or five thoracic sympathetic ganglia
dall, Pace, Wechsler and Kim, ’69) and the gave rise to small filaments that ran independently and directly toward the heart,
baboon.
A further interesting question regarding and occasionally (as reported by Riegele)
the direct action of parasympathetic fibers entered the cardiac plexuses. It is doubtful
upon the ventricular musculature would however, that these fibers contribute sigseem to be resolved by the present ex- nificantly to either inotropic or chronoperiments. It is sometimes felt that the tropic regulation of the heart, since in no
direct inhibitory influence of vagal fibers experiment could functional responses be
on ventricular contractile force can be ex- elicited from isolated thoracic ganglionic
plained by the accompanying reduction in segments (figs. 8, 9). This is not to say,
atrial transference of blood to the ven- however, that they could not serve as aftricular chambers, since atrial contrac- ferent pathways from the heart, or that
198
W. RANDALL, J. ARMOUR, D. RANDALL AND 0. SMITH
they may not exert efferent effects on
metabolic and/or vasomotor functions.
LITERATURE CITED
Becker, F. R., and J. A. Grunt 1957 The cervical sympathetic ganglia. Anat. Rec., 127: 1-14.
Burn, J. H., and M. J. Rand 1959 Sympathetic
postganglionic mechanisms. Nature, 184: 163.
Copen, D. L., D. R. Cirillo and M. Vassale 1968
Tachycardia following vagal stimulation. Am.
J. Physiol., 215: 696-703.
Ellison, J. P., and T. H. Williams 1969
Sympathetic nerve pathways to the human heart
and their variations. Am. J. Anat., 124: 149162.
Kuntz, A. 1933 The autonomic nervous system. In: The Anatomy of the Rhesus Monkey
(Macaca mulatta). Chapt. 17. C. G. Hartman,
ed. Williams and Wilkins.
McKibben, J. S.,and R. Getty 1969 A study of
the cardiac innervation in domestic animals:
cattle. Anat. Rec., 165: 141-152.
Mitchell, G . A. G. 1953 Anatomy of the autonomic nervous system. E. and s. Livingstone,
Edinburgh.
Mizeres, N. J. 1955 The anatomy of the autonomic nervous system in the dog Am. J.
Anat., 96: 285-318.
1963 The cardiac plexus in man. Am.
J. Anat., 112: 141-151.
Perman, E., 1924 Anatomische Untersuchungen iiber die Herzenerven bei den hoheren
Saugetieren und beim Menshen, Ztschr. f. Anat.
u. Entwickl., 71: 382-457.
Randall, W. C., J. B. Pace, J. S. Wechsler and
K. S. Kim 1969 Cardiac responses to separate stimulation of sympathetic and parasympathetic components of the vagosympathetic
trunk i n the dog, Cardiologia, 54: 104-118.
Randall, W. C., and W. G. Rohse 1956 The
augmentor action of the sympathetic cardiac
nerves. Circulation Res., 4 : 4 7 0 4 7 5 .
Riegele, L. 1926 uber die Innervation der Hals
und Brustorgane bei einigen Affen, Ztschr. f .
Anat. u. Entwickl., 80: 777-858.
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