Baroreflex mediated control of heart rate and vascular capacitance in trout
Department of Zoology, Göteborg University, Box 463, S-405 30 Gothenburg, Sweden
* Author for correspondence (e-mail: erik.sandblom{at}zool.gu.se)
Accepted 21 December 2004
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Summary |
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Key words: baroreflex, bradycardia, embolectomy catheter, MCFP, tachycardia, teleost, vascular resistance, venous capacitance, rainbow trout, Oncorhynchus mykiss
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Introduction |
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In teleosts, evidence for a cardiovascular baroreflex is circumstantial and
typically stems from secondary observations made during pharmacological
studies. Early workers noticed that injections of adrenaline, which caused a
rapid increase in arterial pressure, also elicited a transient bradycardia
that could be blocked with atropine
(Helgason and Nilsson, 1973;
Randall and Stevens, 1967
;
Stevens et al., 1972
;
Wood and Shelton, 1980
). Owing
to the fact that vascular resistance was pharmacologically manipulated in
these closed-loop studies, conclusions about the vascular limb of the
baroreflex response could not readily be made. Few studies have previously
dealt with the baroreflex in fish, using open-loop techniques that include
both vascular and cardiac responses (see
West and Van Vliet, 1994
, for
an explanation on open-vs closed-loop studies). Farrell
(1986
) used a technique where a
neoprene collar was placed around the head region of unanaesthetized, but
restrained sea ravens Hemitripterus americanus, thus separating the
trunk from the head region. Elevation of the water level above the tail region
induced a rapidly developing bradycardia that could be blocked with atropine.
After returning to the initial water level, a decrease in systemic resistance
associated with a drop in arterial blood pressure was frequently observed. The
smooth muscle relaxant Papaverine did not seem to alter this response and the
author explained the phenomenon as pooling of blood as the vessels resumed
their initial diameter.
The precise location(s) of baroreceptors in the circulatory system in fish
remains to be substantiated (Nilsson and
Sundin, 1998). Using an open-loop system, it was shown in the
anaesthetized carp Cyprinus carpio that an elevation of pressure in
the intrabranchial afferent arteries resulted in a drop in heart rate and
arterial blood pressure (Ristori,
1970
; Ristori and Dessaux,
1970
). Mott (1951
)
obtained the same results using a similar experimental preparation in the eel
Anguilla anguilla. These early observations pointed out the gills as
the primary site for baroreceptor sensitivity in fish, a fact that still seems
to be the general consensus (Nilsson and
Sundin, 1998
).
As previously pointed out, it is well established in mammals that a drop in
arterial blood pressure also results in an increased sympathetic outflow to
venous capacitance vessels. This leads to mobilization of venous blood and an
increased pressure gradient for venous return. Despite the fact that an active
regulation of venous capacitance is present in fish
(Conklin et al., 1997;
Olson et al., 1997
;
Zhang et al., 1998
), there is
no information on the baroreflex control of venous capacitance in fish.
In the present study a non-pharmacological open-loop technique was used to study the cardiac and the vascular limb of the baroreflex in unanaesthetized trout. Continuous measurements of dorsal aortic blood pressure, venous blood pressure and heart rate were conducted during 30 s of post-branchial dorsal aortic occlusion (increased branchial blood pressure) and ventral aortic pre-branchial occlusion (decreased branchial blood pressure). To evaluate the baroreflex control of venous capacitance, mean circulatory filling pressure was measured during zero-flow conditions, immediately following either occlusion.
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Material and methods |
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Instrumentation and surgical procedures
Preliminary studies indicated that post-surgical viability increased
substantially when the instrumentation of the fish was broken up in two steps,
with a short (12 h) recovery period after the first step. Fish that
displayed irregular or abnormal behaviour after recovery were not used for
further instrumentation. The fish were instrumented as detailed below
(Fig. 1).
|
Dorsal aortic cannulation
Fish were randomly collected from the holding tanks and anaesthetized in
MS-222 solution (150 mg l1) buffered with sodium bicarbonate
(300 mg l1). Prior to surgery the fish were weighed and
transferred to an operating table that was covered with water soaked foam
rubber. During surgery a recirculating system at 10°C continuously
irrigated the gills with water containing sodium bicarbonate-buffered MS-222
(150 mg l1 and 75 mg l1,
respectively).
To measure systemic arterial blood pressure the dorsal aorta was cannulated using a heparinized Fogarty thru-lumen embolectomy catheter (model 12TLW803F, Edwards Lifesciences, Irvine, CA, USA) with an outer diameter of 1 mm and a length of 80 cm. The catheter has two lumens, one being connected to an inflatable latex balloon. The second lumen served to give the arterial blood pressure.
A slightly modified method to cannulate the dorsal aorta via the
roof of the buccal cavity by means of a guide wire was used
(Axelsson and Fritsche, 1994).
Approximately 10 mm oftapered PE-50 tubing was fitted onto the tip of the
embolectomy catheter. This gave the catheter a smooth tapered shape and a good
fit to the guide wire, thus facilitating the cannulation procedure. A mark was
made 50 mm from the anterior tip of the embolectomy catheter. The catheter was
advanced into the vessel until the mark was at the level of the entry point,
located at the first pair of gill arches. This served to give an indication of
how far down the length of the dorsal aorta the inflatable balloon was
positioned. This position was below the bifurcation point of the
coelomesenteric artery. The cannulation procedure occasionally caused some
initial hemorrhage, which was stopped by gently pressing on the wound until
the bleeding ceased spontaneously within a few minutes. A bolus of
approximately 1 ml of heparinized (100 IU ml1) saline (0.9%)
was administered following cannulation. The catheter was attached with one
suture, close to the first pair of gill arches. In order to protect the
catheter from mechanical damage from the teeth, the first 10 cm of the
catheter protruding from the tissue was covered with PE-200 tubing. The
catheter was bent at 180° inside the buccal cavity and exteriorized under
the right operculum. Three sutures were used to attach the catheter to the
roof of the buccal cavity along the row of teeth. An additional suture in the
skin was placed posterior to the operculum. The entire dorsal aortic
cannulation procedure typically took around 20 min. Subsequently the fish were
allowed to recover in covered tanks connected to the departmental water
system.
Cannulation of Sinus venosus
Central venous blood pressure was recorded from the Sinus venosus, which
was non-occlusively cannulated. The fish was positioned on its right side. The
left operculum and the gills were carefully retracted and a less than 10 mm
incision, running approximately 45° dorsoventrally was made. Starting
point was on top of the cleithrum, ending posterior to the Vth
gill-free branchial arch. The lateral part of the Ductus of Cuvier was
dissected free using blunt dissection. The vessel was gently pulled, ideally
5 mm, and secured with a 4-0 suture. A small hole was cut in the upper
part of the venous tissue and a heat-bubbled PE-50 catheter was inserted. The
catheter was directed towards the heart and inserted approximately 10 mm into
the sinus. The catheter was secured in the sinus with a 4-0 suture above the
bubble and to the skin with two additional sutures close to the opercular
opening. For further details, see Altimiras and Axelsson
(2004
).
Attachment of ventral aortic probe
An occlusion probe (i.d. 1.8 mm), custom-made from Perspex, was placed
around the ventral aorta (see Fig.
1 for details). The cuff-type probe was equipped with a vascular
occlusion rubber balloon. This was constructed from approximately 1 m of
heat-flared PE-50 catheter that was bent at a right angle approximately 5 mm
posterior to the flared end. The catheter was filled with water and a small
piece of dental latex rubber (model Thin, Dental Dam, Coltène/Whaledent
Inc, USA and Canada) was tied with a 4-0 suture around the flared end. A small
hole was drilled perpendicular to the lumen, using an injection needle (20 G).
Using a round-type dental drill the luminal side of the hole was countersunk
to fit the flared end of the catheter. The free end of the catheter was pulled
through the hole from the luminal side. The flared end was positioned with the
latex rubber facing the lumen, where it was locked from the outside with a
3 mm piece of heat-flared PE-90 tubing. Inflation of the latex rubber
with a syringe resulted in a bubble developing inside the probe lumen, thus
occluding the ventral aorta. On the opposite side of the occlusion device,
another similar hole was drilled. A 20 MHz Doppler flow crystal (Iowa Doppler
products, Iowa City, IA, USA) was glued to the probe. The flow recordings were
only used to help indicate when zero-flow was reached during the occlusion
manoeuvre.
The probe was positioned around the ventral aorta by making an incision on the right side of the isthmus where the aorta was exposed by blunt dissection. A suture was placed around the vessel that was carefully lifted to facilitate placement of the probe. Two lateral sutures collectively secured the Doppler crystal lead and the occlusion catheter to the skin posterior to the operculum.
Attachment of ECG-electrodes
To enable continuous measurements of heart rate also during zero flow
conditions, two custom-made ECG-electrodes were placed percutaneously close to
the heart. Electrodes were made from Grass Stimulatory electrodes (Grass
Instruments, Quincy, MA, USA), modified by cutting the original ending and
replaced with around 30 mm of platinum wire soldered to the bare ends. To
position the electrodes a 0.8 mm injection needle was used to penetrate the
skin approximately 10 mm anterior to the pectoral fins. The platinum wires
were positioned under the skin on either side of the heart and secured with
skin sutures. Finally all leads and catheters were collectively attached to
the back of the fish with a common suture.
After surgery the fish was transferred to a holding chamber, or immediately to the experimental chamber, both connected to the departmental water system. The fish were placed in the experimental chamber at least 24 h prior to experiments. To minimize stress from visual stimuli, all chambers were thoroughly covered with non-transparent black plastic. Experiments were performed 2472 h following surgery.
Experimental protocol
To stimulate branchial baroreceptors with elevated blood pressure the
embolectomy catheter latex balloon, located in the dorsal aorta
(post-branchial occlusion), was inflated for 30 s with approximately 0.5 ml of
air. This gave the inflated balloon an approximate diameter of 6 mm. Post
mortem analysis in combination with the non-pulsatile pattern of the
Pda recording during occlusion (see Figs
3 and
4), revealed that this was
sufficient to occlude the post-branchial portion of the dorsal aorta and
hence, increase the branchial blood pressure. Low branchial blood pressure was
initiated for 30 s by occluding the ventral aorta (pre-branchial occlusion) by
means of the ventral aortic occluder. Complete occlusion, i.e. zero-flow, was
attained by inflating the latex bubble and simultaneously observing when the
ventral aortic flow and the dorsal aortic pressure dropped (Figs
3 and
4). An occlusion period as long
as 30 s was chosen based on the findings of Zhang et al.
(1995), who noticed that
venous reflex responses to cardiac fibrillation in the trout first appeared
after around 10 s. Although this is considerably less than the 2 min of
vascular compression used in the sea raven
(Farrell, 1986
), preliminary
studies revealed that this stimulation was enough to trigger solid cardiac as
well as vascular responses. Heart rate (fH), dorsal aortic
pressure (Pda) and central venous pressure
(Pven) were continuously recorded. Mean circulatory
filling pressure was measured 2 s following pre- or post-branchial occlusion
assuming that most of the venous response to pre- or post-branchial occlusion
still remained, or during control conditions without manipulated branchial
blood pressure. The order of the three manipulations of branchial blood
pressure was randomized and separated by 30 min. To measure MCFP the ventral
aortic occlusion technique, previously described for trout
(Zhang et al., 1998
), was
employed. Zero-flow conditions were obtained by inflating the latex bubble in
the ventral aortic probe for 8 s. This period is generally assumed to be too
short to induce any reflex responses, but long enough to achieve a stable
venous plateau pressure (Zhang et al.,
1995
). During ventral aortic occlusion systemic arterial blood
pressure dropped instantaneously, whereas venous blood pressure increased.
MCFP was subsequently calculated as the average of 2 s of the venous plateau
pressure period, taken between 5 and 7 s of zero flow.
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|
The same protocol was repeated 1.52 h after -adrenergic
blockade with prazosin (1 mg kg1, Pfizer, Sandwich, England)
and, subsequently, 30 min after an additional atropine treatment (1.2 mg
kg1, Sigma, St Louis, MO, USA). Drugs were dissolved in
physiological saline (0.9%, 1 ml kg1) and administered
slowly via the venous catheter. Sham injections with physiological
saline (0.9%, 1 ml kg1) were also done in identical
experiments as previously described.
Equipment and data acquisition
Arterial and venous blood pressures were measured using pressure
transducers (model DPT-6100, pvb medizintechnik, Kirchseeon, Germany)
connected to a 4ChAmp amplifier (Somedic, Hörby, Sweden). The equipment
was calibrated against a static water column, with the water surface of the
experimental chamber serving as baseline. Cardiac output was recorded using a
directional-pulsed Doppler flow meter (model 545C-4, University of Iowa, Iowa
City, IA, USA) connected to the Doppler crystal in the ventral aortic flow
probe. A Grass amplifier (model 7P511K, Grass Instruments, USA) amplified the
ECG-signal and triggered a Tachograph Recorder unit (model 7P44D, Grass
Instruments, Quincy, MA, USA) in order to obtain heart rate. Data were
digitally stored on a PC running a custom made program, General Acquisition
(Labview version 6.01, National Instruments, Austin, TX, USA).
Statistical analysis and calculations:
The heart rate response during ventral or dorsal aortic occlusion was
calculated as the average value of the last 20 s of each occlusion. Mean
values of 120 s before ventral and dorsal aortic occlusion were pooled to
serve as an unstimulated control. For MCFP measurements, the average value of
Pven between 57 s of a short ventral aortic
occlusion was always used (Zhang et al.,
1998). The effect of altered branchial blood pressure or the
effects of pharmacological treatment were evaluated statistically using a
two-tailed Wilcoxon matched-pairs signed-ranks test, with a fiduciary level of
0.05. When multiple comparisons were made a modified Bonferroni-test was
applied (Holm, 1979
).
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Results |
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Changes in vascular capacitance in response to altered branchial blood pressure
Control fish had a routine MCFP of 0.17±0.03 kPa, which increased
significantly to 0.33±0.03 kPa following prazosin treatment and
remained elevated after additional atropine treatment (0.34±0.04 kPa)
(Fig. 2B).
Following pre-branchial occlusion MCFP in the untreated fish, increased
significantly to 0.27±0.03 kPa compared with routine MCFP in control
fish. Blockade of -adrenergic receptors abolished this response since
mean circulatory filling pressure remained unchanged with pre-branchial
occlusion after prazosin as well as prazosin+atropine treatment. However
post-branchial occlusion in the control fish did not significantly alter MCFP
(0.19±0.02 kPa) to routine MCFP. Instead, post-branchial occlusion
significantly decreased MCFP after treatment with prazosin (from
0.33±0.03 kPa to 0.27±0.03 kPa), a response that was unchanged
with further treatment with atropine (from 0.34±0.04 kPa to
0.27±0.03 kPa).
Systemic arterial responses to decreases in branchial blood pressure
Arterial responses to pre-branchial occlusion were evaluated by comparing
the difference in Pda before and immediately after a
ventral aortic occlusion in control and prazosin-treated fish
(Fig. 3).
The average value of Pda in untreated fish after
pre-branchial occlusion was significantly higher (4.0±0.2 kPa) compared
to the average value before occlusion (3.2±0.1 kPa). Blockade of
-adrenoceptors with prazosin reversed the response and left
Pda significantly reduced following pre-branchial
occlusion (2.3±0.1kPa compared to 2.6±0.2kPa in the
control).
Sham experiments
Despite qualitatively equal responses, sham experiments revealed a slight
increase in control values of MCFP and fH after repeated
occlusions (Table 1). The
underlying mechanism to this is unknown, but a host of potential
neuro-endocrine substances could be released during the course of the
experiment. Substances such as arginine vasotocin
(Conklin et al., 1997);
chatecholamines (Zhang et al.,
1998
), endothelin (Hoagland et
al., 2000
) and neuropeptides
(Olson et al., 1997
) are all
known to affect the cardiovascular (including venous) system in fish.
Regarding these technical limitations, normalized gain for the baroreflex was
not calculated. Hence, the following discussion on the cardiovascular
responses to altered branchial pressure and the effects of pharmacological
treatment should be seen in a qualitative context, rather than in absolute
quantitative terms.
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Discussion |
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The complete lack of chronotropic responses to altered branchial blood
pressure after atropine treatment (Fig.
2A), further supports the reflex origin of the response and shows
that baroreflex mediated modulation of heart rate is exclusively cholinergic.
The same conclusion has previously been drawn in other teleosts such as the
eel (Mott, 1951), the carp
(Ristori, 1970
), and the sea
raven (Farrell, 1986
).
Vascular responses to changes in branchial blood pressure
In untreated animals MCFP was significantly higher when it was preceded by
a pre-branchial occlusion compared to the control
(Fig. 2B). We argue that the
drop in branchial blood pressure during the occlusion was detected by
baroreceptor afferents that initiated a reflex stimulation of capacitance
vessels. The complete block of the vascular response to pre-branchial
occlusion by prazosin identifies the -adrenergic system as the major
mediator of reflex control of vascular capacitance in fish.
Capacitance of the vascular system is dependent on smooth muscle tone and
vascular compliance and represents the relationship between contained blood
volume and transmural pressure in a given segment of the vasculature. Given
that around 70% of the total blood volume is contained in the venous
vasculature, with compliance considerably higher than the arterial
circulation, vascular capacitance in mammals is virtually a matter of the
venous system (Pang, 2001;
Rothe, 1993
). The fact that
the compliance ratio between arterial and venous vascular beds in the trout
has been estimated to be at least 1:21
(Conklin and Olson, 1994
) has
lead previous investigators to assume that this assumption is justified for
fish as well (Conklin et al.,
1997
; Olson et al.,
1997
; Zhang et al.,
1995
; Zhang et al.,
1998
). We therefore conclude that the increase in MCFP observed
following pre-branchial occlusion was the result of an active
-adrenergic venoconstriction, serving to mobilize hemodynamically
inactive venous blood into the stressed vascular compartment that builds up
transmural pressure in the vascular system. Since capacitance is determined by
the relationship between vascular compliance and tone it can only be fully
described in terms of pressurevolume capacitance curves, not by a
single number (Olson et al.,
1997
; Pang, 2001
;
Rothe, 1993
;
Zhang et al., 1998
). In the
present study no manipulations of blood volume were performed, as this is
virtually impossible to achieve without stimulating (baro-) reflexes in intact
animals. Capacitance curves could therefore not be obtained and a conclusive
deduction of whether the observed changes in MCFP are due to changes in
compliance and/or tone cannot readily be made
(Olson et al., 1997
;
Pang, 2001
;
Rothe, 1993
;
Zhang et al., 1998
). In dogs,
however, reflex changes in venous capacitance are mainly mediated by changes
in tone and not compliance (Rothe,
1993
). Whether this can be extrapolated to the situation in fish
is yet to be verified.
No significant difference in MCFP after post-branchial occlusion compared
to the control was found in untreated fish
(Fig. 2B). This is somewhat
surprising considering that an adrenergic tonus on the venous capacitance
vasculature is present in trout at rest
(Zhang et al., 1998). Assuming
that baroreceptors are exclusively restricted to the branchial circulation, an
increase in branchial blood pressure should theoretically result in a
decreased adrenergic tone on capacitance vessels, thus decreasing mean
circulatory filling pressure. However, after prazosin treatment a significant
decrease in MCFP after post-branchial occlusion was unmasked, possibly due to
a redistribution of blood into the splanchnic circulation (see below for
further discussion). Similarly, if blood redistribution to the splanchnic
circulation also occurred in the untreated fish, the measured MCFP would have
been expected to be lower after dorsal aortic occlusion as well. This
discrepancy can possibly be explained by the following factors: (1) The MCFP
manoeuvre in itself requires a short ventral aortic occlusion. The
compensatory reflex responses that might occur during this short circulatory
arrest are generally assumed to be negligible
(Rothe, 1993
;
Zhang et al., 1995
). However,
the possibility that the control system became somewhat super-sensitive during
the post-branchial occlusion, which consequently caused the MCFP manoeuvre to
counteract the response to the long occlusion, cannot be ignored. (2)
Furthermore, baroreceptors located downstream to the post-branchial occlusion
might have obscured the response. If so, low dorsal aortic blood pressure
distal to the occlusion might have buffered the effect of an increased
branchial blood pressure and/or splanchnic blood volume redistribution, thus
leaving MCFP unaltered. The significant increase in control MCFP after
prazosin treatment has been observed before in trout (E.S., unpublished) and
in sea bass (E.S., A. P. Farrell, J. Altimiras, M.A. and G. Claireaux,
submitted). This might seem strange considering that capacitance vessels in
the trout are subjected to an
-adrenergic tonus at rest
(Zhang et al., 1998
). In other
words, the capacitance curve was rotated counter-clockwise and shifted
leftward due to a decreased tone and an increased compliance after prazosin
treatment. The increase in MCFP after prazosin in the present study can be due
to a number of factors such as passive fluid uptake when arterial pressure
drops, and/or an increased compensation of some unknown vasoactive systems. In
the study by Zhang et al.
(1998
), 2040 min was
allowed to elapse after prazosin treatment before the vascular capacitance
curves were constructed. We suspect that this recovery might be too short to
obtain a steady state condition. It is possible that the capacitance curve
would be shifted leftward and gradually rotated clockwise as a consequence of
passive fluid uptake after
-adrenergic blockade. This clearly remains
to be substantiated. In the present study at least 1.5 h was applied to obtain
-adrenergic blockade, and indeed an initial decrease in
Pven was generally seen when prazosin was injected, but
when the experiments were performed 1.52 h later central venous
pressure had usually recovered to initial resting values or above.
Arterial resistance was probably also affected by a decrease in branchial
blood pressure during pre-branchial occlusion
(Fig. 3). In untreated animals
dorsal aortic blood pressure was always initially increased after
pre-branchial occlusion, compared to the value before occlusion. After
prazosin treatment this response was completely absent, showing that an
-adrenergic response was responsible for this response. These findings
are in line with previous findings in the anaesthetized carp
(Ristori, 1970
), but different
from the study on the sea raven (Farrell,
1986
), where no change in arterial conductance was seen after
vascular compression.
Integration of chronotropic and vascular responses
The time course of the chronotropic and the vascular responses to
manipulations of branchial blood pressure appear to differ considerably
(Fig. 4). After pre-branchial
occlusion the changes in heart rate start within seconds. By contrast, venous
pressure first appears to plateau at MCFP before slowly increasing as a
consequence of reflex venoconstriction
(Rothe, 1993; Zhang et al.,
1995
,
1998
). The physiological
relevance of this would be that the changes in heart rate, and possibly also
systemic resistance, mainly provide beat-to-beat fine-tuning of arterial blood
pressure. This might in part serve as an effective means of protecting the
delicate respiratory epithelium in the gills
(Van Vliet and West, 1994
).
The process of blood mobilization from the venous circulation operates on a
slightly larger time scale. In terrestrial animals subjected to gravitational
forces, the necessity of venoconstriction during orthostatic challenges as a
means of providing sufficient venous return is obvious. However, in aquatic
animals that live in a near gravity-free environment, it is somewhat more
difficult to visualize how such reflexes have evolved. Various explanations
for the necessity of active venoconstriction in aquatic vertebrates have been
presented. Ogilvy and DuBois
(1982
) noticed that bluefish
Pomatomus saltatrix tolerated head-up tilting and could maintain
arterial blood pressure. This ability was described as an adaptation of the
vascular system to counteract hydrodynamic forces acting on the vasculature
during swimming. It is also known that trout can actively mobilize venous
blood in order to compensate for blood loss during haemorrhage
(Duff and Olson, 1989
). In
mammals it is well known that MCFP increases when cardiac output is increased.
This is believed to reflect an increase in the upstream venous (venular)
driving pressure for venous return, which evidently has to increase when
cardiac output is increased (Pang,
2001
; Rothe,
1993
). Cardiac output was the manipulated variable in the present
study and therefore we cannot say whether it was increased or not. However,
when cardiac output (and venous return) is increased during exercise in the
European sea bass Dicentrarchus labrax there is a significant
increase in MCFP, suggesting that regulation of venous capacitance is a
general and highly important mechanism in the control of cardiac output in
fish (E.S., A. P. Farrell, J. Altimiras, M.A. and G. Claireaux,
submitted).
Location of baroreceptors
Although the barosensitive properties of the branchial circulation in fish
are generally accepted, it is fascinating to note that the vascular and the
cardiac responses to alterations in branchial blood pressure not necessarily
operate in concert. For example, the lack of response (or decrease) in
vascular capacitance with an associated bradycardia after post-branchial
occlusion (Fig. 2A,B) in the
untreated fish, raise the question of whether extra-branchial baroreceptors
are involved in the control of cardiovascular homeostasis. It is tempting, but
somewhat premature, to speculate that gill-receptors mainly control the
cardiac chronotropic limb of the baroreflex, as has previously been shown
using open-loop techniques in anaesthetized fish
(Mott, 1951;
Ristori, 1970
;
Ristori and Dessaux, 1970
),
whereas additional baroreceptors located downstream possibly also mediate the
vascular responses. It should be emphasized, however, that the consistent
chronotropic responses to pre- and post-branchial occlusion in the present
study, do not necessarily leave the gills as the sole location for
baroreceptors controlling heart rate in fish. Potential post-branchial
receptors would also have been affected by the occlusions.
Further studies are clearly needed. Due to anatomical constraints,
open-loop studies similar to those used in toads, where gradual occlusion
distal or proximal to various barosensitive areas enabled measurement of
normalized gain, are possibly not applicable in the trout (for two
comprehensive reviews, see Van Vliet and
West, 1994; West and Van
Vliet, 1994
). Finding alternative experimental fish species where
the large systemic vessels are surgically accessible could be the key to
further understanding.
Methodological evaluation
Embolectomy catheters, which are normally used in clinical situations for
treatment of arteriosclerosis, might be a valuable experimental tool in a
variety of research situations in the field of comparative cardiovascular
physiology. Preliminary studies revealed that an accurate placement of the
occlusion balloon down the length of the dorsal aorta was crucial for a
successful occlusion manoeuvre. If the balloon was positioned at the
bifurcation of the celiacomesenteric artery, balloon inflation inevitably
ruptured the vessel wall. Hence, in the experimental series the balloon was
advanced further distal to the bifurcation where inflation did not induce any
visible damage. This might have resulted in a net redistribution of blood into
the splanchnic circulation during dorsal aortic occlusion. At least in
mammals, the gut vasculature has a high capacitance, and the hepatic
circulation a comparably large resistance
(Rothe, 1993). Also in fish
the entire gastrointestinal blood flow passes through the hepatic circulation
before it empties into the central venous system
(Thorarensen et al., 1991
). A
net shift of blood into the splanchnic circulation during dorsal aortic
occlusion could therefore result in a decrease in mean circulatory filling
pressure as measured in the central veins. In order to verify that branchial
blood pressure actually increases during dorsal aortic occlusion, a ventral
aortic catheter could have been used. Since the present experimental approach
already demands fairly extensive instrumentation this was not done in an
attempt to minimize surgical stress. Considering that 6080% of cardiac
output is distributed to the systemic arterial circulation at rest
(Farrell et al., 2001
), we feel
confident that dorsal aortic occlusion produces enough increase in branchial
blood pressure to stimulate potential barosensitive areas. A potential problem
that arises when branchial outflow is transiently occluded is the fact that
not only is branchial blood pressure increased, but presumably also blood
pressure in the central nervous system. Although neither abnormal behavioural
responses nor increased mortality, indicative of brain damage, were observed
even after repeated occlusions, the potential effects of this cannot be
ignored.
Concluding remarks
Bagshaw (1985) postulated
that there has been an evolutionary transition amongst the vertebrates
regarding the baroreflex. Regulation of cardiovascular homeostasis in the
teleosts was claimed to be mainly heart-rate-based, whereas a more refined
system including both cardiac and vascular properties first appears in the
higher vertebrates. However, these arguments are not easy to reconcile,
considering that our study clearly demonstrates that stimulation or unloading
of baroreceptors in the trout not only results in chronotropic responses but
also in profound changes in vascular capacitance and systemic resistance, very
similar to the situation in mammals. As Jones and Milsom
(1982
) pointed out the
baroreflex is likely to be a phylogenetically ancient cardiovascular trait
that evolved well before vertebrates became subjected to gravitational forces
when terrestrial habitats were colonized. Our findings further support this
view by showing that both the cardiac and the vascular limbs of the baroreflex
are important for the maintenance of cardiovascular homeostasis in fish.
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Acknowledgments |
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References |
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