AMER. ZOOL., 27:111-120(1987)
The Reptilian Baroreceptor and Its Role in
Cardiovascular Control1
PHILIP J. BERGER
Monash University Centre for Early Human Development,
Queen Victoria Medical Centre, Melbourne, Victoria 3000, Australia
SYNOPSIS. Anatomical evidence for the existence of a depressor nerve in reptiles was
first reported 100 years ago. Electrical stimulation of the central end of the cut nerve,
however, did not produce an unequivocal fall in heart rate and blood pressure, so it was
thought not to function as a depressor nerve. This remained the state of knowledge for
fifty years when Marco Fedele performed a superb anatomical and physiological study of
the depressor nerves of turtles and lizards. He demonstrated that there were two depressor
nerves from each vagus; the superior nerve originated from the jugular ganglion or
superior laryngeal nerve in turtles and from the superior laryngeal nerve or vagus in
lizards; the inferior nerve originated from the nodose ganglion or slightly caudad of this
ganglion. The nerves were shown to terminate in the proximal truncus arteriosus. Unlike
the earlier workers, Fedele obtained a clear depressor effect on stimulating the depressor
nerves.
In more recent times baroreflexes have been demonstrated in response to hemorrhage
and body tilting in reptiles, with snakes receiving particular attention. The evidence
indicates that aquatic snakes are less effective at maintaining blood pressure than terrestrial
and arboreal forms. The sensitivity (gain) of the baroreceptor-heart rate reflex, when it
is expressed as a percentage change in heart rate per unit pressure change, is approximately
the same in reptiles, amphibians, and mammals. In addition, the ultrastructural appearance
of the baroreceptors of lizards is similar to that of mammals. A quantitative assessment
of the ability of reptiles to correct disturbances in blood pressure has not yet been made,
but techniques for obtaining this information are now available.
running between the aorta and pulmonary
artery to reach "the heart on the arterial
side instead of on the venous side. This
nerve is in all probability the homologue
of the N. depressor in other animals." In
Testudo graeca they also found a depressor
nerve originating from a ganglion (presumably the jugular) high in the neck (Fig.
1); in addition they refer to a "rather strong
branch from the vagus [entering] the heart
with the large arterial vessels," although
the title depressor was not given to this
nerve. Gaskell (1886, p. 20) later described
a depressor nerve in Crocodilus biporcatus.
Mills (1884) similarly reported on the existence of a depressor in Testudo cephalo which
corresponds to that from the jugular
ganglion described by Gaskell and Gadow.
On anatomical grounds therefore there
appeared to be a depressor nerve in reptiles. However, central stimulation of the
depressor nerve led Mills (1885) to conclude that it was not functionally homologous with the same nerve in mammals.
1
From the Symposium on Cardiovascular Adaptation Kazem-Beck (1885, 1888) came to a similar
in Reptiles presented at the Annual Meeting of the conclusion.
American Society of Zoologists, 27—30 December
1984, at Denver, Colorado.
The negative physiological findings
INTRODUCTION
That powerful mechanisms exist for
altering blood pressure was revealed when
Cyon and Ludwig (1866) showed that central stimulation of a branch of the vagus
nerve caused a fall in blood pressure and
heart rate in the rabbit. This nerve, aptly
called the "depressor," originated from the
vagus high up in the neck and, according
to Cyon and Ludwig, reached the ventricles by way of the aortic root. It was some
time before a nerve considered to be the
homologue of the depressor of the rabbit
was found in reptiles. Among the first to
report on the subject was W. H. Gaskell
whose observations were no doubt influenced by the year he spent working in Ludwig's laboratory in 1874 (see Pike, 1914;
Sharpey-Schafer, 1927, p. 33). Gaskell and
Gadow (1884) described a slender nerve
arising from the ganglion trunci vagi
(nodose) of Alligator mississipiensis and then
111
112
PHILIP J. BERGER
Glossopharyngeal n.
- — Jugular g.
Sympathetic n
\—Sympathetic n.
Vagus n.
Depressor n.
Nodose g.
FIG. 1. Origin of depressor nerve in the turtle Testudo graeca according to Gaskell and Gadow (1884).
The depressor reached the heart via the cervical sympathetic nerve, but it could be traced to its origin
from the jugular ganglion.
threw doubt on the existence of a depressor nerve in reptiles even though the
admittedly scanty anatomical evidence suggested that such a nerve did exist. To
resolve the question a detailed study was
clearly necessary. Promise that such a study
was to be performed was given by Gaskell
and Gadow (1884) who said that they
intended to extend their "investigations
over all the chief groups of vertebrata, to
decide whether cardiac nerves with separate functions as depressors, accelerators
and inhibitors, is an intrinsic universal
character of the vertebrate cardiac system." Considering his elegant demonstration in turtles that the heart beat is a
myogenic phenomenon (Gaskell, 1883) and
that the sympathetic and vagal nerves of
frogs and crocodiles have separate excitatory and inhibitory effects on the heart
(Gaskell, 1884), the promise to fully investigate the depressor nerves could well have
seen the establishment of their territory of
distribution being worked out first in a reptile. As it turned out Gaskell did not return
to the subject, perhaps because circumstances brought about by his wife's illness
diverted his interest to a study of the origin
of the vertebrates (see Pike, 1914; Sharpey-Schafer, 1927, p. 34). That the depres-
Truncus Arteriosus
FIG. 2. Anatomy of truncal nerves in Testudo graeca:
redrawn according to Fedele (1937). This illustration
shows the origins of the superior and inferior nerves
from the dorsal aspect.
sor nerves do not reach the heart, but distribute to the aortic arch and base of the
right subclavian artery was first established
by Koster and Tschermak (1902, 1903) in
dogs. As to the reptilian depressor, 50 years
elapsed after Gaskell's work before it again
attracted serious study.
ANATOMY
Depressor nerves
By the time that Marco Fedele published
his huge study of the reptilian depressor
nerves in 1937 (not 1935 as is generally
stated) it was already known that pressuresensitive receptors existed in the carotid
sinus of mammals (Hering, 1923, 1924).
Fedele's work, however, concentrated upon
the depressor nerves. This was fortunate,
for, as we shall see later, there is no evidence for baroreceptors in reptiles at the
site homologous with the mammalian
carotid sinus, and it is questionable whether
Fedele could have as splendidly performed
the enormous job of tracing the depressors
and also investigated the innervation of the
region homologous with the carotid sinus.
Fedele showed that there are two distinct
depressor nerves to the truncus arteriosus
on each side of the animal; these he referred
REFLEX CONTROL OF CARDIOVASCULAR SYSTEM
113
Internal Carotid a.
Superior Laryngeal n.
Vagus n.
Superior Truncal n.
Ductus Caroticus
Nodose Ganglion
Sympathetic n.
Lateral Aorta
Inferior Laryngeal n.
Inferior Truncal n
Inferior Truncal n.
Atria
Ventricle'
FIG. 3. Dorsal view of the origin and course of truncal nerves in Lacerta, redrawn from Fedele (1937).
to as the superior and inferior truncal to the description of Gaskell and Gadow
nerves. In turtles (Emys orbicularis and Tes- (1884) can be seen by comparing Figures
tudo graeca) the superior truncal nerve 1 and 2. Gaskell and Gadow depict a single
originates as one, two or sometimes more depressor nerve originating from the jugbranches from the superior laryngeal nerve ular ganglion while Fedele adds as well the
or jugular ganglion (Fig. 2). In lizards inferior nerve. As mentioned earlier Gas{Lacerta viridis and Lacerta muralis) the kell and Gadow described another branch
superior truncal nerve originates low in the to the truncus but did not call it a depresneck as one or two branches from the supe- sor; this probably corresponds to the inferior laryngeal nerve or that nerve and the rior nerve of Fedele and possibly was not
vagus (Fig. 3). The inferior nerve in turtles considered to be a depressor because there
originates from the nodose ganglion at the is only a single depressor nerve in mammals
base of the neck while in lizards it is just arising from the jugular ganglion, and Gasbelow that ganglion slightly craniad of the kell would have been well aware of this
fact.
recurrent laryngeal nerve.
Just as the mammalian depressor nerve
The course followed by the superior
truncal nerve differs in turtles and lizards. does not reach the ventricles, according to
In the former the nerve follows the neu- Fedele the reptilian truncal nerves do not
rovascular bundle (vagus, jugular vein, cross the bulbar ring but distribute to the
carotid artery) to the base of the neck and proximal truncus (Fig. 4). This finding has
then runs onto the central arteries (Fig. 2). been verified in the lizard Trachydosaurus
In the latter it runs directly to the central rugosus (Berger et al., 1982) with the minor
arteries which lie close to its origin (Fig. exception that a small branch reaches the
3). Once the superior and inferior nerves dorsal surface of the ventricle. In spite of
reach the truncus arteriosus they form a Fedele's work, in the snake Vipera berus
common plexus, with the left truncal nerves (Boyd, 1942), and in the lizard Uromastyx
preferentially innervating the ventral trun- aegyptia (Khalil and Malek, 1952), the truncus and the right truncal nerves distrib- cal nerves were reported to originate in the
uting predominantly to the dorsal surface. ventricle. Being in Italian, Fedele's work
Branches from both sides innervate the does not appear to have been widely read.
internal walls of the truncus.
When the proximal truncus arteriosis of
The extent to which Fedele (1937) added T. rugosus was examined with electronmi-
114
PHILIP J. BERGER
Superior Truncal n.
Internal Carotid a.^
/
|nferior
T r u n c a
,
n.
/
Lateral Aorta
Subclavian a.
Pulmonary a.
Bulbar Ring
Coronary a.
Truncus Arteriosus
FIG. 4. Ventral view of the distribution of truncal nerves to the proximal truncus arteriosus of Emys orbiculans,
redrawn from Fedele (1937). The original (Fedele's fig. 17) shows the nerves on the right side distributing
to the dorsal surface of the truncus.
croscopy it was found to be innervated by
a variety of nerve profiles (Berger et al.,
1982), with one group resembling very
closely those found in the mammalian
carotid sinus (e.g., Bock and Gorgas, 1976;
Krauhs, 1979). These profiles, with diameters up to 7 fim, had an irregular shape
and cytoplasm packed with mitochondria,
myelin whorls, glycogen and large and small
vesicles (Fig. 5). This evidence indicates that
baroreceptors probably have similar morphology in reptiles and mammals. The
truncus of reptiles also contains large numbers of chromaffin cells with a rich innervation (Trinci, 1912; Adams, 1962; Furness and Moore, 1970; Berger et al., 1982)
suggesting that it might be important in
chemoreception as well as baroreception.
Indeed the location of the region embryologically homologous with the mammalian sinus is not entirely agreed upon for
all reptiles. Adams (1958, 1962) remains
the authority on this question, and while
snakes might be an exception (see later),
the region may be considered to lie at the
base of the neck, close to the nodose ganglion of the vagus nerve. This region is
innervated by vagal and possibly glossopharyngeal fibres (Terni, 1931; Adams,
1939,1942,1952,1957; Chowdhary, 1950;
Oelrich, 1956; Mehra, 1958; Rogers,
1967).
PHYSIOLOGY
Central stimulation of the truncal nerves
produced a fall in blood pressure and heart
rate in turtles and lizards, while peripheral
"Carotid sinus" nerves
stimulation had no effect (Fedele, 1937).
A baroreceptive role for the mammalian Fedele concluded that these nerves were
carotid sinus was shown by Hering (1923, comparable in action to the aortic depres1924) and since then there have been sev- sor nerve of mammals. The existence of
eral reports of similar anatomical arrange- truncal baroreceptors has since been conments at sites thought to be homologous firmed by the fall in heart rate produced
in reptiles. There is, however, no distinct by raising intratruncal pressure by inflacarotid sinus in reptiles: i.e., there is no tion of a perivascular cuff occluder in T.
region where the artery dilates and the rugosus (Berger et al., 1980; Fig. 6). The
media of the vessel is reduced or absent evidence became complete when Faraci et
and the adventitia is heavily innervated. al. (1982) recorded baroreceptor dis-
REFLEX CONTROL OF CARDIOVASCULAR SYSTEM
115
FIG. 5. Large, presumed sensory nerve profile in the outer media of the left aortic root in the proximal
truncus (from Berger et al., 1982). The profile is packed with mitochondria and lysosomes. Scale bar = 2 /im.
charge from vagal filaments in Pseudemys
scripta and localized the receptive endings
by punctate stimulation to the "bulbus cordis and proximal pulmonary artery." Baroreceptors with afferent projections in the
vagus nerve have also been reported by
Kamenskaya et al. (1977).
The involvement of the carotid bifurcation (in reptiles without a ductus caroticus) or trificuration (in those with a ductus) in baroreceptor-mediated reflexes has
never been demonstrated. It might be considered premature to conclude that the
region does not contain baroreceptors
because only one study has produced evidence that heart rate is unaffected by a fall
in pressure in the common carotid arteries
(Berger et al, 1980; Fig. 7). The case is
somewhat strengthened by reference to
unpublished observations showing that the
"carotid sinus reflex does not seem to exist
in iguanas" (Hohnke 1975). In addition, in
turtles it appears that the "carotid sinus"
is not innervated by the vagus or the glossopharyngeal nerves, and as a result could
not participate in baroreceptor-mediated
reflexes. Furthermore, there is no evidence in amphibians (Ishii and Ishii, 1978;
Segura, 1979) or birds (see Jones and
Johansen, 1972) that the region homologous with the mammalian carotid sinus
contains baroreceptors. The simplest
hypothesis is that a baroreceptor role for
the carotid sinus developed de novo in mammals or their synapsid reptilian precursors.
SENSITIVITY OF BAROREFLEXES
Several techniques have been used in an
attempt to assess the effectiveness with
which the reptilian baroreflex maintains a
constant blood pressure in the face of disturbances. The first examines how well
116
PHILIP J. BERGER
2min
truncus
truncus
truncus
Fie. 6. Effect of raising intratruncal pressure (P car. aortic) by inflating for the time indicated by the thick
bar a peri vascular occluding cuff placed around the distal truncus in T. rugosus (from Berger et al., 1980). In
A, heart rate (HR) fell abruptly and returned to about the control level once the cuff was deflated. In B and
C heart rate overshot control at the time the animal began to struggle.
blood pressure is maintained during progressive hemorrhage (Hohnke, 1975;
Lillywhite and Smith, 1981; Lillywhite
and Pough, 1983; Lillywhite et al., 1983).
Results indicate that blood pressure is
actively maintained during hemorrhage in
lizards and snakes, with aquatic snakes
being considerably less effective than terrestrial forms. T h e second technique
involves tilting the animals to examine the
control of blood pressure (Hohnke, 1975;
Seymour and Lillywhite, 1976; Lillywhite
and Seymour, 1978; Lillywhite and Pough,
1983).
The idea behind this technique is that
with the head pointed upwards a hydrostatic gradient is imposed from the head
to the tail; pressure rises at the tail end and
falls at the head end. Results indicate that
heart rate and peripheral resistance are
altered in response to tilting, and that terrestrial and arboreal snakes more effectively restore blood pressure towards the
control value. However, as they have been
performed so far, tilting experiments do
not provide us with a strictly quantitative
measure of the sensitivity of the baroreflex
control of blood pressure and heart rate.
The reason is that tilting constitutes a complex cardiovascular stimulus. During a
head-up tilt for instance, given that pres-
sure falls at the head and rises at the tail,
there must be a point somewhere along the
body where pressure does not change; this
is known as the hydrostatic indifferent point
(HIP), and as Gauer and Thron (1965)
make clear this point can have a different
location in humans in the head-up and
head-down position. Thus, tilting will provide a quite different stimulus (pressure
change) to the baroreceptors of different
species if their baroreceptors lie at substantially different distances from the HIP.
Seymour and Lillywhite (1976) present evidence that in terrestrial and arboreal snakes
the heart is near the head, whereas it lies
closer to the mid-body of aquatic forms.
As Jones and Milsom (1982) point out,
assuming that the baroreceptors of snakes
lie in the proximal truncus and that the
HIP is near the mid-body, tilting would
stimulate the baroreceptors of aquatic
snakes far less than terrestrial and arboreal
species.
While recognising that the complexity
of the tilt stimulus makes it difficult to
derive an estimate of baroreflex sensitivity
from tilting experiments, two points may
be made based on present evidence. Since
postural changes in aquatic species would
not change transmural pressures in the vasculature, whereas of course they would in
117
REFLEX CONTROL OF CARDIOVASCULAR SYSTEM
2min
Paorta
30
HR
20
common carotids
vena cava
FIG. 7. Lack of response to lowering pressure at the "carotid sinus" homologue in T. rugosus (from Berger
et al, 1980). In A cuffs around left and right common carotid arteries were inflated for the time indicated
by the bar. Pressure in the ductus caroticus (P d. car) fell while that in the aorta (P aorta) was relatively
unaffected. Heart rate did not change. In B pressure in the carotid system and aorta were similarly affected
by inflating a cuff around the inferior vena cava and heart rate increased substantially.
terrestrial and arboreal species, these
experiments demonstrate that the species
that most need to counteract the effects of
posture on blood pressure are those most
able to do so. The second point is that it
is probably no coincidence that in nonaquatic snakes the heart, and presumably
the baroreceptors, lie close to the head to
ensure that cephalic driving pressure is
maintained when the animal changes posture.
After arguing the non-quantitative
nature of tilting experiments, Jones and
Milsom (1982) pointed out that Boyd (1942)
considered the carotid bifurcation to be a
baroreceptor site in snakes. If this is so, the
location of the heart might be unimportant
and tilting might then provide a quantitative estimate of baroreflex sensitivity. It
seems unnecessary to weaken the argument in this way for several reasons. The
innervation of the internal carotid artery,
according to Boyd (1942) is "only slightly
branched" and in this respect "the fibres
differ markedly from [those] found in the
carotid sinus . . . of . . . mammals." Secondly, Adams (1958) favored the view that
the carotid bifurcation, which Boyd (1942)
described at the base of the skull, is secondary, and therefore not homologous with
the mammalian carotid bifurcation. Finally,
even in a reptile with a persistent ductus
caroticus, where there can be no dispute
about the location of the carotid sinus
homologue, lowering intravascular pressure at this site had no effect on heart rate
(Berger et al., 1980; Fig. 7). In summary,
the technique of body tilting should be
treated with some caution when assessing
the relative sensitivity of the baroreflex in
species of vastly differing body forms; to
do so satisfactorily it would be necessary to
quantify the change in pressure brought
about at the baroreceptors by tilting, and
to determine the extent to which this pressure is returned to its control value.
Quite apart from the evidence from body
tilting experiments, other techniques confirm that aquatic snakes less effectively control blood pressure than terrestrial forms.
Thus during hemorrhage, blood pressure
was at best poorly maintained when volume reductions were small in two aquatic
species; as an approximation it could be
said that pressure fell linearly with blood
loss (Lillywhite and Pough, 1983). In addition, raising blood pressure with epinephrine or norepinephrine, and lowering it
with acetylcholine, produced smaller compensating changes in heart rate than in ter-
118
PHILIP J. BERGER
restrial species (Lillywhite and Pough, Evidence in mammals (Boettcher et al.,
1983). Unfortunately, as well as affecting 1978; Vatner and Boettcher, 1978; Anderperipheral vessels, these drugs have pow- son et al., 1979) suggested that under resterful direct effects on the heart which might ing conditions this assumption is true. As
to an extent have masked the cardiac for reptiles, virtually the entire cardiac outresponse to the imposed pressure change. put change during exercise in Iguana
Two studies have been performed which iguana, and in Varanus exanthematicus
enable us to compare the strength of the approximately 80% of it, is achieved by
reptilian baroreflex with other tetrapods. increases in heart rate (Gleeson et al., 1980).
Millard and Moalli (1980), using nitroglyc- However, as Berger et al. (1980) point out,
erin to lower blood pressure and phenyl- if we wish to know "the comparative ability
ephrine to raise it, showed that heart period of animals to regulate blood pressure, a
(reciprocal of heart rate) changed twice as more useful gain to measure is that relating
much in turtles {Pseudemys scripta elegans)changes in central arterial pressure and
as in frogs (Rana catesbeiana). By contrast, changes in pressure at the isolated baroin a similar study, Stephens et al. (1983) receptor site. In this value, total peripheral
reported a barely perceptible heart rate resistance and heart output both particiresponse to imposed blood pressure pate." This is an elementary point although
changes in Pseudemys and Chrysemys. In the Jones and Milsom (1982) make the extraorsecond study Berger et al. (1980) used peri- dinary claim that studies of the comparavascular cuffs to raise and lower blood pres- tive efficacy of barostatic control suffer a
sure. Determining the gain of the baro- number of problems "not the least of which
reflex in terms of change in heart period seems to be the lack of the realization that
per unit change in pressure produced an baroreceptors control blood pressure and
estimate of 1,370 ms/kPa (100 ms/mm Hg) not heart rate, stroke volume or peripheral
in T. rugosus while the value for rabbits is resistance."
5.2 ± 1.0ms/mmHg(Korner <?/«/., 1972).
A major problem in designing a study of
The vast difference in these two values is baroreflex control of blood pressure in
almost entirely accounted for by the hyper- reptiles arises from the actual location of
bolic relationship between heart rate and the receptors. Lying as they do in the proxheart period; the same proportional fall in imal truncus arteriosus, it is impossible to
heart rate for a unit pressure change pro- isolate them surgically from the remainder
duces a larger gain in an animal with low of the circulation in order to manipulate
heart rate than in one with a high rate. the pressure to which they are exposed
Normalizing gain by calculating it as per- while determining the magnitude of the
centage change in heart rate per unit pres- resultant pressure change in the general
sure change produced values of 7.2%/mm circulation. Such a study would yield the
Hg in T. rugosus compared with 2-5% in open-loop gain of the baroreflex, an
three mammals (Berger et al., 1980) and a important variable in control systems thevalue of approximately 1% in the toad Bufo ory, and a value readily available for mammarinus (Smith et al., 1981). Thus blood mals. There are methods, however, by
pressure changes in a variety of tetrapods which the open-loop gain can be estimated
have approximately the same effect on from closed-loop studies, as Sagawa (1983)
heart rate.
has discussed. For ethical reasons such
The physiological significance of an esti- techniques are the only ones available for
mate of baroreflex sensitivity incorporat- studying humans where the circulation
ing only the cardiac component of that must remain intact. Two of the techniques
reflex was considered by Berger et al. are those of hemorrhage and body tilting.
(1980). They argued that proportional It seems likely, therefore, that with careful
changes in heart rate would indicate how attention to experimental design the very
effectively cardiac output could be altered techniques now most commonly used to
to maintain constant pressure, if stroke vol- study reptilian barostasis could provide an
ume were to remain relatively constant. estimate of the open-loop gain of the baro-
REFLEX CONTROL OF CARDIOVASCULAR SYSTEM
119
der sensibilen Nerven des Herzen auf die motorischen Nerven der Blutgefasse Ber. Saechs. Ges.
Akad. Wiss. 18:307-328.
Faraci, F. M., H. W. Shirer, J. A. Orr, and J. W.
Trank. 1982. Circulatory mechanoreceptors in
the pond turtle Pseudemys scripta. Am. J. Physiol.
242(Regulatory Integrative Comp. Physiol. 11):
R216-R219.
Fedele, M. 1937. I nervi del tronco arterioso nel
quadro della innervazione cardiaca nei Rettili e
il problema del 'depressore' nei Vertebrata. Mem.
R. Ace. Naz. Lincei. ser. 6, 6(1934-1937):387520.
Furness, J. B. and J. Moore. 1970. The adrenergic
ACKNOWLEDGMENTS
innervation of the cardiovascular system of the
I thank Daphne Hards for tirelessly
lizard Trachysaurus rugosus. Z. Zellforsch 108:ISOtranslating Fedele and for the enormous
Gaskell, W. H. 1883. On the innervation of the heart,
amount of work she did for this article.
with especial reference to the heart of the tortoise. J. Physiol. (London) 4:43-127.
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