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First published online December 16, 2008
Journal of Experimental Biology 212, 145-151 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.024042
The unequal influences of the left and right vagi on the control of the heart and pulmonary artery in the rattlesnake, Crotalus durissus
1 Departmento de Zoologia, Universidade Estadual Paulista, Rio Claro, SP,
Brazil
2 School of Biosciences, The University of Birmingham, Edgbaston B15 2TT,
UK
3 Institute of Biology, Aarhus University, 8000 Aarhus C, Denmark
* Author for correspondence (e-mail: E.W.Taylor{at}bham.ac.uk)
Accepted 28 August 2008
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pul) and
cardiac shunt patterns are primarily controlled by the parasympathetic nervous
system. The vagus innervates both the heart and a sphincter on the pulmonary
artery. The present study reveals that whereas both the left and right vagi
influence fH, it is only the left vagus that influences
pulmonary vascular resistance. This is associated with the fact that
rattlesnakes, in common with some other species of snakes, have a single
functional lung, as the other lung regresses during development. Stimulation
of the left cervical vagus in anaesthetised snakes slowed the heart and
markedly reduced blood flow in the pulmonary artery whereas stimulation of the
right cervical vagus slowed the heart and caused a small increase in stroke
volume (VS) in both the systemic and pulmonary
circulations. Central stimulation of either vagus caused small (5–10%)
reductions in systemic blood pressure but did not affect blood flows or
fH. A bilateral differentiation between the vagi was
confirmed by progressive vagotomy in recovered snakes. Transection of the left
vagus caused a slight increase in fH (10%) but a 70%
increase in pul, largely
due to an increase in pulmonary stroke volume (VS,pul).
Subsequent complete vagotomy caused a 60% increase in fH
accompanied by a slight rise in
pul, with no further change
in VS,pul. By contrast, transection of the right vagus
elicited a slight tachycardia but no change in VS,pul.
Subsequent complete vagotomy was accompanied by marked increases in
fH, pul
and VS,pul. These data show that although the heart
receives bilateral vagal innervation, the sphincter on the pulmonary artery is
innervated solely by the left vagus. This paves the way for an investigation
of the role of the cardiac shunt in regulating metabolic rate, as chronic left
vagotomy will cause a pronounced left–right shunt in recovered animals,
whilst leaving intact control of the heart, via the right vagus.
Key words: cardiovascular, nervous control, reptile
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).
Although there was clear evidence of chronotropic adrenergic control of the
heart in rattlesnakes, inhibitory vagal control was predominant
(Wang et al., 2001b). The
vagus nerve in vertebrates, including reptiles, runs to the heart, trachea,
lungs, pulmonary and coronary vasculature as well as other visceral organs
such as the digestive tract. In reptiles, peripheral electrical stimulation of
the vagus or intravenous injection of acetylcholine results both in
bradycardia and an increase in pulmonary vascular resistance, which reduces
pulmonary blood flow (pul)
(Burggren, 1977a;
Burggren, 1977b;
Milsom et al., 1977;
Hicks, 1998). This is because
the heart and a sphincter on the pulmonary artery are innervated by the vagus,
which terminates on muscarinic cholinoceptors
(Luckhardt and Carlson, 1921).
Efferent activity in the vagus slows the heart and causes constriction of the
sphincter on the pulmonary artery, which shunts blood away from the lungs [a
right-to-left (R–L) cardiac shunt]. Thus, the net direction and
magnitude of shunt flow is largely determined by changes in resistance in the
pulmonary circuit, relative to the systemic circuit, due to active vagal,
cholinergic regulation of pulmonary arterial resistance
(Hicks, 1994). Reptiles are
typically periodic breathers. During apnoea, resistance in the pulmonary
circuit is increased, resulting in a marked R–L cardiac shunt whereas
during bouts of breathing, a reduced resistance in the pulmonary circuit can
increase blood flow to the lungs [a left-to-right (L–R) cardiac shunt]
(see Wang et al., 2001b).
Thus, vasomotor control is important in diverting blood between the pulmonary
and systemic systems (Woodbury and
Robertson, 1942) and may even enable an increase in oxygen demand
to be satisfied in the absence of increased lung ventilation
(Wang and Hicks, 1996).
Complete vagotomy in the rattlesnake caused heart rate
(fH) to rise and become unvarying, and the breathing
rhythm to become very slow, with very large tidal volumes
(Wang et al., 2001a). These
data were interpreted as loss of vagal tone on the heart, which is known to be
responsible for fH variability as well as setting
fH plus denervation of lung stretch receptors, with the
resultant loss of the Hering–Breuer reflex
(Sundin et al., 2001;
Wang et al., 2001b;
Campbell et al., 2006), In a
series of exploratory experiments it became apparent that the left and right
vagi were not equal in their mediation of these classic responses. This may
relate to the fact that the rattlesnake, in common with some other species of
snakes, only possesses a single functional lung. Thus, the vagal afferent
innervation of lung receptors and efferent innervation of the sphincter on the
pulmonary artery may be similarly unilateral. The present study sought to
quantify these differences.
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MATERIALS AND METHODS |
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Experimental protocols
Vagal stimulation in anaesthetised snakes
These experiments were designed to investigate putative differences between
the left and right vagi with respect to their cardiovascular control. All
procedures were in accordance with the ethical requirements imposed on animal
experimentation in Brazil and were based on the standards applied in Denmark
and the UK. Eight snakes were terminally anaesthetised with the
pentobarbiturate, Mebumal (20 mg kg–1), injected into the
caudal vein. The snakes normally lost all behavioural reflexes within 15 min
and were then placed in a supine position. A ventrolateral incision was made
immediately above the heart to expose the central blood vessels. A cannula (PE
60 containing heparinised saline) was inserted into the right aortic arch
(RAO) via the occluded vertebral artery, for measurements
of blood pressure. We placed transonic blood flow probes (2R or 2S depending
on the size of the snake) around the main branch of the pulmonary artery and
around the left aortic arch (LAO) to measure pulmonary blood flow
(pul) and left aortic blood
flow (LAO). All
cardiovascular variables stabilised quickly after completion of the surgery
and base-line data were obtained for up to 30 min before proceeding to
stimulate the vagus nerves.
The cervical vagus was exposed on either side via another ventral
midline incision in the neck, and both vagi were dissected free from
connective tissue, so that they could be lifted onto platinum hooks for
electrical stimulation (Physiological Stimulator, Farnell Instruments,
Wetherby, UK). Peripheral stimulation consisted of positive-going 2 ms stimuli
delivered at frequencies between 0.2 and 70 Hz at 2–10 V, depending on
the measured responses obtained from each preparation. The appropriate
stimulation voltage was determined by progressively increasing voltage until a
maximal response was obtained at a frequency eliciting changes in
fH and/or changes in
pul. A range of
frequency–response determinations was then made for each nerve. Each
stimulation was followed by a period of recovery that constituted the control
conditions for the subsequent stimulation. The same stimulation parameters
were then retained for subsequent central stimulation of the same nerve. In
four animals, atropine (3 mg kg–1) was injected and allowed
to take effect for 15 min before peripheral vagal stimulation was repeated to
investigate whether the haemodynamic responses had been blocked.
Effects of vagotomy on cardiovascular variables in fully recovered snakes
Given that stimulation of the right and left vagi in anaesthetised snakes
revealed pronounced differences in the effects on
pul, we aimed to
characterise the effects of sectioning the left or right vagus on central
vascular blood flows and fH in fully recovered snakes. To
implant blood flow probes and snares around the vagi, ten snakes were
anaesthetised by inhalation of CO2. This method of anaesthesia has
been used many times on reptiles and induces lack of movement and
insensitivity to physical stimulation such as handling for 4–10 min in
rattlesnakes (Wang et al.,
1993). During anaesthesia the snakes were hypoxaemic and acidotic
but plasma acid–base status and oxygen levels returned to normal values
within 2 to 6 h (Wang et al.,
1993). Furthermore, rattlesnakes subject to operative procedures
under CO2 anaesthesia, have survived for several weeks, feeding and
acting normally. One ventrolateral incision, 5–7 cm long, was made
cranial to the heart, so that one Transonic blood flow probe (2R, 2S or 1.5S
depending on the size of the animal) could be placed around the left pulmonary
artery. The site of each incision was injected with xylocaine as an analgesic.
While the left lung of Crotalus is completely reduced, the right lung
is perfused by the left pulmonary arch
(Van Bourgondien and Bothner,
1969). Consequently,
pul can be readily assessed
by placement of a single blood flow probe around the left pulmonary artery.
Another probe was then placed around the LAO. The leads of each
probe were secured to the skin with a single suture and exteriorised from the
animal through the incision, which was closed with intermittent sutures.
Another ventral mid-line incision was made in the neck and snares, made of
3–0 silk suture (Kruuse A/S, Marslev, Denmark), were placed around the
left and right vagi and exteriorised on the back of the snake. All snakes
resumed spontaneous ventilation within 30 min of completion of the operative
procedures and appeared to regain normal behavioural patterns within a few
hours. All snakes were held in 60 cmx30 cmx15 cm plastic boxes at
24–28°C and allowed to recover overnight.
On the following day, blood flows and fH were allowed to stabilise for one to two hours after connecting the probes to the flow meter. The snare surrounding one of the vagi was then pulled, with minimum disturbance to the unanaesthetised snake. After this unilateral vagotomy, blood flows were allowed to stabilise over the next 30–60 min, while measurements were taken. Complete vagotomy was then achieved by pulling the remaining snare. In five snakes, the left side was vagotomised before the right side whereas an opposite order of vagotomy was performed in the other five snakes.
Measurements of blood pressure, fH and blood flows
Systemic arterial blood pressure (Psys) was measured by
connecting the systemic arterial catheter to a Baxter Edward (model PX600,
Irvine, CA, USA) disposable pressure transducer. The signals from the pressure
transducers were amplified using an in-house built pre-amplifier and were
calibrated daily against a static column of water. The blood flow probes were
connected to a Transonic dual channel blood flow meter (T206) for measurements
of instantaneous blood flow rates. Data were collected electronically using a
Biopac 100 acquisition package and analysed using AcqKnowledge data analysis
software (v. 3.7.1; Biopac, Goleta, CA, USA).
Statistical analysis
The effects of left or right vagal stimulation on the relative changes in
haemodynamic variables were analysed with a one-way analysis of variance
(ANOVA) for repeated measures. A one-way ANOVA for repeated measures was also
applied to assess the effects of uni-lateral and subsequent complete vagotomy
on haemodynamic variables. Effects were considered significant whenever
P<0.05.
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RESULTS |
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LAO (see
Galli et al., 2005b) that
allows for an estimation of cardiac shunt patterns, which is expressed as
pul/sys.
In the fully recovered snakes, a small net L–R cardiac shunt prevailed
whereas the anaesthetised snakes were characterised by a small net R–L
cardiac shunt.
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Effects of vagal stimulation in anaesthetised snakes
The cardiovascular changes elicited by electrical stimulation of the
efferent vagus differed substantially between the right and left vagi. Thus,
although stimulation of either side led to pronounced reductions in
fH, stimulation of the left vagus also led to large
reductions in pul. An
experimental recording from one experiment, shown in
Fig. 1, highlights these
differences. The records depict similar reductions in fH
following stimulation of the right or left vagi. The bradycardia elicited by
electrical stimulation of the right vagus was associated with an increase in
Vs in both the systemic and pulmonary circulations. By
contrast, a similar bradycardia during left vagal stimulation was associated
with a marked and progressive reduction in the VS to the
pulmonary circulation whereas the increased VS to the
systemic circulation resembled the response to right vagal stimulation.
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A similar response was observed in all nine animals and the means of the combined data are illustrated in Fig. 2. In this figure, we present the changes in systemic and pulmonary stroke volumes, as well as Psys, during moderate reductions (to approximately 60%) and maximal reductions (to approximately 20%) in fH, arising from different rates of stimulation of the left or the right vagi. Regardless of which of the vagi was stimulated, Psys decreased and VS,sys increased as a proportion of the decrease in fH. Although VS,pul increased slightly on stimulation of the right vagus, it decreased significantly on stimulation of the left vagus, independently of the reduction in fH, implying pulmonary vasoconstriction.
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Afferent central stimulation of either side of the vagus was performed in five snakes. In none of the animals did we observe changes in fH or blood flow but small 5–10% reductions of systemic blood pressure were observed in some animals.
Effects of vagotomy on haemodynamic variables in fully recovered snakes
The differential actions of the left and right vagi were also evident from
the cardiovascular changes that followed from selective vagotomy of either the
right or left side in recovered snakes
(Fig. 3). Transection of the
left vagus, while leaving the right vagus intact, elicited a small but
significant increase in fH of approximately 10%
(Fig. 3C) but was associated
with a 70% increase in pul,
while LAO was not affected
(Fig. 3A,B). The increased
pul could largely be
ascribed to an elevated VS,pul
(Fig. 4A). Subsequent complete
vagotomy caused a 60% increase in fH accompanied by a
slight rise in pul, with no
further change in VS,pul
(Fig. 4A). By contrast,
transection of the right vagus, leaving the left vagus intact, elicited a
small increase in fH and
pul but no change in
VS,pul. Subsequent complete vagotomy, following
transection of the left vagus, was accompanied by marked increases in
fH, pul
and VS,pul
(Fig. 3A,D;
Fig. 4C), indicating that the
left vagus plays a predominant role in controlling pulmonary blood flow.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). This accords with our finding that stimulation of the left
vagus reduced pul. However,
Wallach, (Wallach, 1998),
quoting other historical sources (e.g.
Butler, 1895), stated
emphatically that Cope was mistaken and that snakes typically retain the right
lung. This apparent paradox was solved by Van Bourgondien and Bothner
(Van Bourgondien and Bothner,
1969). Their careful study of the arterial systems of crotalid
snakes showed that the `right' (sic) lung was effectively perfused by
the left pulmonary artery. Their detailed description of the topography of the
major arteries surrounding the heart match our observations during the
placement of flow probes around the pulmonary artery and the
LAO.
Blood flows, Psys and fH of the
anaesthetised snakes are similar to previous studies on this species using a
similar preparation (Galli et al.,
2005a; Galli et al.,
2005b; Galli et al.,
2007; Hagensen et al.,
2008). However, fH and
pul of fully recovered
snakes were lower than snakes anaesthetised with pentobarbital
(Table 1). A similar effect has
been observed in turtles and rattlesnakes
(Crossley et al., 1998;
Skals et al., 2005).
Rattlesnakes equipped with data loggers for ECG that had recovered from
anaesthesia for 120 h, carrying ECG electrodes attached to a data logger so
that they were unrestrained, showed progressive recovery of
fH to nocturnal lows around 12 beats
min–1 (Campbell et al.,
2006). Thus, in the present study the combined implantation of
flow probes and vagal snares seems to have reduced the extent of postoperative
recovery of cardiac vagal tone. However, partial recovery was clearly achieved
as pulling the snares increased fH and had differential
left/right effects on
pul.
The vagus nerve exerts several important functions in the regulation of
cardio–respiratory function in vertebrates and our study confirms this
role in a reptile. On the efferent side, the vagus innervates the heart,
smooth muscle surrounding the pulmonary artery as well as smooth muscle in the
lungs. In Crotalus, the action of the vagus on the heart was
confirmed by the observation that peripheral electrical stimulation of the
vagus caused a pronounced bradycardia in anaesthetised snakes and that
vagotomy led to a marked tachycardia in fully recovered snakes, indicating
that the heart operates under a degree of vagal tone. Similarly, stimulation
of the vagus as well as vagotomy elicited large changes in
pul. However, our study
documents a pronounced unequal influence of the vagi on either side of the
animal on pulmonary blood flow, whilst the vagi on both sides have similar
influences on fH. This observation is novel.
Bilateral differences in vagal efferent control on the heart have been
reported in turtles (Gaskell,
1882; Mills, 1885;
Garrey, 1911) and in isolated
Langendorff perfused rabbit hearts, where stimulation of the right vagus
causes larger reductions in fH than the left vagus
(Ng et al., 2001). Hicks and
Comeau found that electrical stimulation of the right vagus of a turtle
induced greater reductions in fH and
pul than stimulation of the
left vagus (Hicks and Comeau,
1994). However, the responses of the heart and the pulmonary
circulation were qualitatively similar
(Hicks and Comeau, 1994). In
anaesthetised Crotalus, stimulation of either vagus slowed the heart
but pul was controlled
solely by the left vagus. These observation are supported by vagotomy in
recovered snakes where denervation of the left vagus caused large increases in
pul and
VS,pul whereas
pul was unaffected by
vagotomy on the right side. When the right side was denervated after the left
side, there was nevertheless a further increase of
pul. Although this could
indicate a release of remaining tone on the pulmonary artery, it seems more
likely that the rise in pul
is caused by the elevated fH, where the increased cardiac
output is directed into the low resistance circuit of the pulmonary
circulation.
The vagal influence on the heart in Crotalus is consistent with
numerous studies on different reptiles and other vertebrates, showing cardiac
slowing upon vagal stimulation or infusion of acetylcholine (e.g.
Gaskell, 1882;
De la Lande et al., 1962;
Kirby and Burnstock, 1969;
Berger, 1971;
Hedberg and Nilsson, 1975;
Burggren, 1977a;
Burggren, 1977b;
Milsom et al., 1977;
Wojtaszek, 1979;
Donald et al., 1990b;
Comeau and Hicks, 1994;
Hicks and Comeau, 1994). As
the vagus releases acetylcholine onto muscarinic cholinoceptors on the heart,
its influence is antagonised by atropine (e.g.
Burnstock, 1969;
Hedberg and Nilsson, 1975;
Berger and Burnstock, 1979;
Morris and Nilsson, 1994).
Although other neurotransmitters have been implicated in control of the heart
in reptiles (Donald et al.,
1990a; Lillywhite and Donald,
1994; Wang et al.,
2001a), in Crotalus, atropine completely blocked the
reduction in fH during vagal stimulation. Furthermore,
fH after complete vagotomy (47.8±2.6
min–1 for all 12 snakes) was almost identical to the value of
48.3±1.1 min–1 that was observed in Crotalus
after infusion with atropine (T.W., A.S.A. and E.W.T., unpublished
observations). Thus, it seems that efferent control of fH
by the vagus in Crotalus can be attributed solely to the release of
acetylcholine.
In reptiles, the vagus normally runs together with sympathetic nerves, in a
mixed vagosympathetic nerve, so that vagotomy by nerve transection will result
in removal of sympathetic tone as well as vagal tone on the heart. In some
reptiles, fH increases during electrical stimulation of
the vagus following treatment with atropine, which has been interpreted as
release of an adrenergic neurotransmitter from sympathetic nerves
(De la Lande et al., 1962;
Hedberg and Nilsson, 1975).
This was not observed in Crotalus, although this species exhibits
clear chronotropic responses to β-adrenergic stimulation
(Skals et al., 2005). The
heart in Crotalus operates under a degree of inhibitory vagal tone
that overrides a smaller sympathetic tonus
(Wang et al., 2001a;
Wang et al., 2001b).
Furthermore, Galli and colleagues showed that the degree of adrenergic
regulation of the pulmonary circulation is relatively small in
Crotalus (Galli et al.,
2007).
The absence of a pronounced effect of central stimulation of the vagus
nerve is surprising as the vagus carries information from oxygen sensitive
chemoreceptors on the aortic arches as well as stretch and CO2
sensitive receptors within the lungs. Sundin and colleagues recorded lung
stretch receptor responses from the peripheral cut end of the vagus in snakes
(Sundin et al., 2001). Vagal
innervation of pulmonary stretch receptors (PSRs) was also revealed by a
pronounced increase in tidal volume following complete vagotomy
(Wang et al., 2001a;
Wang et al., 2001b).
Stimulation of these and other vagal inputs, such as those from baroreceptors,
would be expected to cause changes in cardiovascular variables
(Hicks and Comeau, 1994). At
present, we cannot offer a convincing explanation for why this was not
observed in the rattlesnake, although changes would be mediated in part
via the vagus nerve and the centrally stimulated branch was
transected in this preparation.
The inhibitory role of vagal activity on
pul in Crotalus is
consistent with previous studies on a range of reptiles
(Burggren, 1977a;
Burggren, 1977b;
Milsom et al., 1977;
Donald et al., 1990a;
Donald et al., 1990b;
Hicks and Comeau, 1994).
Although the present study cannot reveal the precise location of the vagal
regulation of pulmonary vascular resistance, it shows clearly that it is on a
portion of the pulmonary artery that is innervated solely by the left vagus.
In turtles, the vagus innervates smooth muscle on the main pulmonary artery
(Burggren, 1977a;
Milsom et al., 1977) and in
the garter snake, Thamnophis, the innervation appears to be very
close to the heart (Burggren,
1977b). Acetylcholine is recognised as the major neurotransmitter
for the vagal innervation of the pulmonary circulation in a number of reptiles
(Donald et al., 1990a;
Donald et al., 1990b;
Hicks, 1998) but
non-adrenergic-non-cholinergic (NANC) regulation has been reported in the
garter snake (Smith and Mcintyre,
1979).
Very little is known about the normal patterns of cardiac shunting in
snakes and although some species possess prominent ventricular pressure
separation (Wang et al.,
2003), others can exhibit sizeable cardiac shunts
(Lillywhite and Donald, 1989).
Crotalus does not possess pressure separation between the systemic
and pulmonary arteries (Galli et al.,
2005a; Galli et al.,
2005b) and large R–L cardiac shunts at low temperatures have
been inferred from arterial oxygen levels
(Wang et al., 1998). The very
large increase in pul with
no attendent changes in sys
certainly indicates that L–R cardiac shunts can be very large in
Crotalus. We did not measure blood flows in systemic arteries other
than the LAO but we are able to estimate
sys using the flow
distribution among the systemic arches of anaesthetised Crotalus
measured in a previous study (Galli et
al., 2005b). On this basis, we estimate that the net cardiac shunt
(pul–sys)
of resting undisturbed Crotalus is rather small but that a net
L–R shunt dominates. In turtles and toads, a net R–L shunt
normally prevails in resting undisturbed animals and the development of a net
L–R shunt is normally associated with exercise or hypoxia
(West et al., 1992;
Wang and Hicks, 1996;
Wang et al., 1997;
Wang et al., 1998;
Gamperl et al., 1999;
Wang and Hicks, 2002).
The physiological consequences of cardiac shunts in reptiles have been
discussed for more than a century but it remains uncertain whether the ability
to mix systemic and venous blood within the ventricle confers functional
advantages (see Burggren, 1987;
Hicks and Wang, 1996;
Wang and Hicks, 2008). The
many unresolved issues can, at least partially, be ascribed to the lack of
good animal candidates on which we could manipulate cardiac shunts, without
incurring unwanted side effects, and then measure long-term effects in
performance (e.g. exercise, growth, digestion, etc.). The differential
regulation of pul by the
left and right vagi in Crotalus raises an interesting possibility of
using this species to study some functional consequences of cardiac shunts.
Unilateral transection of the vagus did not cause major changes in
fH (Fig.
3C,F), which suggest that the other side remained functional and
capable of maintaining an adequate tone on the heart. Thus, it is likely that
unilaterally vagotomised Crotalus would retain the ability to exhibit
normal fH responses to altered metabolic demands. However,
upon left vagal denervation, the remaining right vagus would not exert neural
control of pulmonary vascular resistance. Under such conditions,
pul would be determined
exclusively by fH as well as humoral and local influences
on vascular resistances, which appear to be rather small in the pulmonary
circulation of Crotalus (Galli et
al., 2005a; Galli et al.,
2005b; Galli et al.,
2007). As a result, denervation of the left vagus is expected to
chronically abolish the ability of Crotalus to reduce
pul. It would be
interesting to investigate whether this inability affected measurable
physiological parameters such as minimal and maximal metabolic rate,
temperature selection and lung fluid homeostasis, and whether in the long run
appetite and growth rate were affected.
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Berger, P. J. (1971). The vagal and sympathetic innervation of the heart of the lizard Tiliqua rugosa. Aust. J. Exp. Biol. Med. Sci. 49,297 -304.[CrossRef][Medline]
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Burggren, W. W. (1977a). The pulmonary circulation of the chelonian reptile: morphology, haemodynamics and pharmacology. J. Comp. Physiol. 116,303 -323.
Burggren, W. W. (1977b). Circulation during intermittent lung ventilation in the garter snake Thamnophis. Can. J. Zool. 55,1720 -1725.[CrossRef]
Burggren, W. W. (1987). Form and function in reptilian circulations. Am. Zool. 27, 5-19.
Burnstock, G. (1969). Evolution of the
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Butler, G. W. (1895). On the complete or partial suppression of the right lung in the Amphisbaenidae and of the left lung in snakes and snake-like lizards and amphibians. Proc. Zool. Soc. Lond. 1895,691 -712.
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S., Egginton, S., Rantin, F. T., Bishop, C. M. and Taylor, E. W.
(2006). Evidence for a respiratory component, similar to
mammalian respiratory sinus arrhythmia, in the heart rate variability signal
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Comeau, S. G. and Hicks, J. W. (1994). Regulation of central vascular blood flow in turtle. Am. J. Physiol. 36,R569 -R578.
Cope, E. D. (1894). On the lungs of the ophidia. Proc. Am. Philos. Soc. 33,217 -224.
Crossley, D., Altimiras, J. and Wang, T. (1998). Hypoxia elicits an increase in pulmonary vasculature resistance in anaesthetised turtles (Trachemys scripta). J. Exp. Biol. 201,3367 -3375.[Abstract]
De la Lande, I. S., Tyler, M. J. and Pridmore, B. R. (1962). Pharmacology of the heart of Tiliqua [Trachysaurus] rugosa (the sleepy lizard). Aus. J. Exp. Biol. 40,129 -138.[CrossRef]
Donald, J. A., O'Shea, J. E. and Lillywhite, H. B. (1990a). Somatostatin and innervation of the heart of the snake Elaphe obsoleta. Am. J. Physiol. 27,R1001 -R1007.
Donald, J. A., O'Shea, J. E. and Lillywhite, H. B. (1990b). Neural regulation of the pulmonary vasculature in a semi-arboreal snake, Elaphe obsoleta. J. Comp. Physiol. 159B,677 -685.
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