Cardiorespiratory adjustments during hypercarbia in rainbow trout Oncorhynchus mykiss are initiated by external CO2 receptors on the first gill arch
Department of Biology, University of Ottawa, 50 Marie Curie, Ottawa, Ontario, Canada, K1N 6N5
* e-mail: sfperry{at}science.uottawa.ca
Accepted 5 August 2002
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Summary |
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To assess whether the CO2 chemoreceptors of the first gill arch were sensing water and/or blood PCO2, bolus injections of CO2-enriched water or saline were made into the buccal cavity or caudal vein, respectively. Injections of CO2-enriched water to preferentially stimulate external receptors evoked catecholamine release and cardiorespiratory responses that closely resembled the responses to hypercarbia. As in hypercarbia, extirpation of the first gill arch prevented the bradycardia and the increase in ventilation amplitude associated with externally injected CO2-enriched water. Except for a slight decrease in cardiac frequency (from 73.0±2.8 to 70.3±3.5 beats min-1; N=11), injection of CO2-enriched saline to preferentially stimulate internal chemoreceptors did not affect any measured variable. Taken together, these data indicate that, in rainbow trout, the bradycardia and hyperventilation associated with hypercarbia are triggered largely by external CO2 chemoreceptors confined to the first gill arch.
Key words: hypercarbia, catecholamine, chemoreceptor, chromaffin cell, gill, fish, rainbow trout, Oncorhynchus mykiss, cardiovascular, respiration, bradycardia
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Introduction |
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The predominant site of O2 chemoreception in fish is the first
gill arch (Burleson et al.,
1992; Fritsche and Nilsson,
1993
). Current models of cardiorespiratory control
(Burleson, 1995
;
Milsom et al., 1999
) contend
that the cardiovascular responses to altered environmental O2
levels are initiated by externally oriented receptors whereas the ventilatory
responses are triggered by external and internal receptors. Therefore, by
analogy with the situation in mammals, in which the peripheral O2
and CO2 chemoreceptors share a common location
(O'Regan and Majcherczyk,
1982
), the present study was designed to test the hypothesis that
the CO2 chemoreceptors in trout are predominantly localised to the
first gill arch. Additional experiments were performed to assess the potential
involvement of externally and internally oriented receptors.
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Materials and methods |
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Animal preparation
All experimental protocols (including surgical procedures; see below) were
previously approved by the University of Ottawa Animal Care Committee in
accordance with guidelines provided by The Canadian Council for Animal Care.
Fish were anaesthetised in a solution of benzocaine (0.1 gl-1
ethyl-p-aminobenzoate; Sigma) and placed onto an operating table
where the gills were ventilated with a solution of the anaesthetic. To permit
measurement of arterial blood pressure (Pa), a polyethylene cannula
(Clay Adams, PE 50) was implanted into the dorsal aorta via
percutaneous puncture of the roof of the buccal cavity
(Olson et al., 1997). To
sample arterial blood or to inject drugs or CO2-enriched saline
into the pre-branchial circulation, cannulae (PE 50) were implanted into the
caudal artery and vein, respectively, using standard surgical procedures
(Axelsson and Fritsche, 1994
).
Access to the caudal vessels was achieved by an incision lateral to the spinal
cord slightly caudal to the anal fin. In those fish to which
CO2-enriched water was administered across the gills (see below), a
delivery cannula (PE 160) was placed into the mouth through a hole in the
snout.
To enable measurement of cardiac output, a small (1.5 cm) midline ventral
incision was made to expose the pericardial cavity, and the pericardium was
dissected away to expose the bulbus arteriosus. A 3S or 4S ultrasonic flow
probe (Transonic Systems, Ithaca, NY, USA) was placed non-occlusively around
the bulbus. Lubricating jelly (K-Y Personal Lubricant; Johnson and Johnson
Inc.) was used with the perivascular flow probe as an acoustic couplant. Silk
sutures were used to close the ventral incision and to anchor the cardiac
output probe lead to the skin. Small brass plates (1 cm2) were
sutured to the external surface of each operculum to allow the measurement of
ventilation parameters by means of an impedance converter
(Peyraud and Ferret-Bouin,
1960).
In those experiments in which the first gill arches were removed, the arches were initially ligated dorsally and ventrally and then removed with scissors. This procedure removed the entire respiratory surface of the gill arch; all that remained was a tiny stump at either end that was subsequently cauterised.
Following surgery, fish were placed into individual black Plexiglas boxes supplied with flowing, aerated water and were allowed to recover for 24h prior to experimentation.
Experimental protocol
Series 1: effects of hypercarbia
These experiments were performed on intact (N=16), gill-extirpated
(N=12) and atropine-treated (1 µmol kg-1; N=7)
fish; different fish were used in each group. Once blood pressures and
water/cardiovascular values had stabilized, an initial blood sample (0.5 ml)
was withdrawn from the caudal artery cannula. After 10 min of normocarbic
normoxia, the water supplying the fish box was rendered hypercarbic for 20 min
by gassing a water equilibration column with 1.5% CO2 in air
(Cameron flowmeter model GF-3/MP). The desired target water
PCO2 (PWCO2) of
8 mmHg (1 mmHg = 0.133 kPa) was controlled by adjusting the rates of water
and/or gas flow thorough the equilibrium column. A second blood sample (0.5
ml) was withdrawn at maximum hypercarbic exposure, immediately prior to
switching the inflow water back to normocarbic normoxia; a final blood sample
was take 20 min later.
Series 2: effects of external CO2
These protocols were performed on intact (N=22) and
gill-extirpated (N=11) fish. Experiments commenced with a 10 min
recording period under normoxic, normocarbic resting conditions. After this
pre-treatment period, air-equilibrated (controls) or CO2-enriched
(5% CO2) water was injected (50 ml kg-1) into the buccal
cannula to deliver a bolus of water to the gills. The injections were
delivered over a 20 s period; fish continued to breathe during the injection
period. Blood samples were removed via the caudal artery cannula
immediately prior to injection of CO2-enriched water and 2 min
thereafter. As discussed by Perry and McKendry
(2001), it was estimated that
the PCO2 of the water flowing over the lamellae
would be approximately 10 mmHg after mixing and dilution by inspired water
(PWCO2
0.5 mmHg).
Series 3: effects of internal CO2
Intact trout (N=8) were injected via the caudal vein
cannula with saline (140 mmoll-1 NaCl; 2 mlkg-1)
pre-equilibrated with 5% CO2. Assuming negligible interconversion
between CO2, HCO3 and H+ within the brief
period of transit to the gill, mixing of the injected saline with the venous
blood was estimated to yield a final PCO2 of
9.0 mmHg (for further details, see Perry
and McKendry, 2001). Blood samples were taken prior to and 2 min
after injection of saline. Control fish (N=8) were injected with 2
mlkg-1 of air-equilibrated saline. Owing to the absence of any
marked effects of internal injections on cardiorespiratory function or plasma
catecholamine levels, these experiments were not repeated on gill-extirpated
fish.
Analytical procedures
Measurement of plasma catecholamine concentrations
All blood samples collected for measurements of catecholamine
concentrations were centrifuged immediately at 12000 g for 1
min and flash-frozen in liquid N2 before being placed in storage at
-80°C. Plasma noradrenaline and adrenaline levels were determined on
alumina-extracted samples (200 µl) using high-pressure liquid
chromatography (HPLC) with electrochemical detection
(Woodward, 1982). The HPLC
consisted of a Varian Star 9012 solvent delivery system (Varian Chromatography
Systems) coupled to a Princeton Applied Research 400 electrochemical detector
(EG&G Instruments). The extracted samples were passed through an
Ultratechsphere ODS-C18 5 µm column (HPLC Technology Ltd), and
the separated amines were integrated with the Star Chromatography software
program (version 4.0, Varian). Concentrations were calculated relative to
appropriate standards and with 3,4-dihydroxybenzylamine hydrobromide (DHBA) as
an internal standard in all determinations.
Measurement of water gas tensions
A pump-driven loop continuously withdrew inflowing water and passed it over
PO2 and PCO2
electrodes (Radiometer) housed in temperature-controlled cuvettes (13°C)
and connected to a Radiometer blood gas analyser. The
PO2 electrode was calibrated by pumping a zero
solution (2 gl-1 sodium sulphite) or air-saturated water
continuously through the electrode sample compartments until stable readings
were recorded. The PCO2 electrode was
calibrated in a similar manner using mixtures of 0.5% and 1.0% CO2
in air provided by a gas-mixing flowmeter (Cameron Instruments). The
electrodes were calibrated prior to each individual experiment.
Measurement of cardiorespiratory variables
The dorsal aortic cannula was flushed with heparinised saline (100 i.u.
ml-1) to prevent clotting and then connected to a pressure
transducer (Bell and Howell) precalibrated against a static column of water.
Analog blood pressure signals were measured using Harvard Biopac amplifiers
(DA 100). Cardiac output was determined by connecting the ultrasonic flow
probe to a small animal blood flow meter (T106, Transonic Systems, Ithaca, NY,
USA). All flow probes were pre-calibrated in the factory using diluted
mammalian blood (haematocrit 25%) at 13°C. The frequency and amplitude of
opercular displacements were assessed as indices of ventilation using a
custom-built impedance converter that detected and quantified the changes in
impedance between the brass plates attached to the opercula
(Peyraud and Ferret-Bouin,
1960). All analog signals (water gas tensions, impedance values
and cardiac output,
b) were converted
to digital data and stored by interfacing with a data-acquisition system
(Biopac Systems Inc.) using Acknowledge data-acquisition software (sampling
rate 30 Hz) and a Pentium personal computer. Thus, continuous data recordings
were obtained for mass-specific
b,
cardiac frequency (fH; automatic rate calculation from the pulsatile
b trace), cardiac stroke volume
(
S;
b/fH), ventilation frequency
(fG; automatic rate calculation from the raw ventilation impedance
traces), ventilation amplitude (VAMP; the difference
between maximum and minimum impedance values), mean blood pressure (arithmetic
mean) and systemic vascular resistance (RS; mean
Pa/
b).
Statistical analyses
The data are reported as means ± 1 standard error of the mean
(S.E.M.). All data were statistically analysed by a two-way repeated-measures
analysis of variance followed by a post-hoc multiple-comparison test
(Bonferroni t-test). The limit of statistical significance was
5%.
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Results |
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Series 2: effects of external CO2
The effects of injecting CO2-enriched water into the buccal
cavity are depicted in Fig. 4.
In the intact fish, externally applied CO2 caused a reduction in
fH and b as well as increases
in Pa, RS, VAMP and plasma
catecholamine levels (Table 2);
fG was unaffected. Except for the reduction in
b, these results closely resembled the
cardiorespiratory responses to hypercarbia (see above). Extirpation of the
first gill arch prevented the bradycardia, the decline in
b and the increase in
VAMP associated with externally injected
CO2-enriched water; all other responses were unaffected by gill
extirpation.
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Series 2: effects of internal CO2
The injection of CO2-enriched saline into the caudal vein
(Fig. 5) caused only minor
changes in the measured cardiorespiratory variables: an increase in
Pa and a slight, but significant, bradycardia (from 73.0±2.8
to 70.3±3.5 beats min-1). The increase in Pa was
also observed in fish injected with air-equilibrated saline, suggesting that
this response (as well as an increase in
b) was a consequence of vascular
volume loading. To ensure that the administered saline was reaching putative
internal chemoreceptive sites, a bolus of sodium cyanide (0.1 mg
kg-1) was injected into the caudal vein. This procedure resulted in
a marked increase in plasma catecholamine levels
(Table 3) as well as initiating
marked cardiorespiratory reflexes (fH declined from 74.4±2.7
to 38.3±6.0 beats min-1 and VAMP
increased from 0.53±0.07 to 0.72±0.05 cm; S. G. Reid and S. F.
Perry, unpublished data). These data indicate that the injected saline was at
least reaching sites of O2 chemoreception.
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Discussion |
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There was no attempt in the present study to discern between the specific
effects of CO2 versus H+ in the initiation of
cardiorespiratory responses to hypercarbia. However, despite some earlier
indirect evidence for H+ reception in fish
(Heisler et al., 1988;
Graham et al., 1990
;
Wood et al., 1990
), the
results of more recent studies that have attempted to distinguish between
CO2 and H+ receptors are consistent with receptors that
are predominantly activated by changes in extracellular
PCO2
(Sundin et al., 2000
;
Reid et al., 2000
;
Perry and McKendry, 2001
).
Regardless, as in mammals (Gonzalez et
al., 1992
), the proximate stimulus for CO2
chemoreception is likely to be a decrease in the intracellular pH of the
chemosensory cells (Gilmour,
2001
).
In the presence of elevated ambient CO2 tensions, trout exhibit
bradycardia, increased arterial blood pressure (caused by an increase in
systemic resistance) and an elevation of ventilation amplitude. This pattern
of cardiorespiratory adjustment in response to CO2, while
consistently observed in salmonids (Perry
et al., 1999; McKendry and
Perry, 2001
; for a review, see
Perry and Gilmour, 2002
),
varies markedly among the other species that have been examined. For example,
bradycardia, while exhibited by several species, is not displayed by channel
catfish (Ictalurus punctatus;
Burleson and Smatresk, 2000
),
white sturgeon (Acipenser transmontanus;
Crocker et al., 2000
) or
American eel (Anguilla rostrata; see
Table 1 in
Perry and Gilmour, 2002
) and
thus cannot be considered a universal response to hypercarbia. Similarly,
there is marked inter-specific variation in the blood pressure responses to
hypercarbia spanning almost all possible response patterns (see
Table 2 in
Perry and Gilmour, 2002
).
Although hyperventilation is a common response to elevated ambient
PCO2
(Gilmour, 2001
), the
sensitivity of the response varies amongst species, with some fish (e.g.
trout) exhibiting a high degree of sensitivity
(Thomas, 1983
) and other (e.g.
carp Cyprinus carpio) displaying relative insensitivity
(Soncini and Glass, 2000
).
Two previous studies have attempted to localise CO2
chemoreceptors to the first gill arch. Sundin et al.
(2000) demonstrated that
hypercarbic bradycardia in tambaqui was mediated exclusively by
first-gill-arch receptors whereas ventilatory responses were probably caused
by stimulation of chemoreceptors on all arches. In contrast, the elevation of
blood pressure during hypercarbia in tambaqui appeared to involve stimulation
of extrabranchial receptors because the response persisted in fish
experiencing total gill denervation
(Sundin et al., 2000
). Reid et
al. (2000
), however, were
unable to provide any evidence for specific first-gill-arch CO2
receptors in traira and concluded that the hyperventilation and bradycardia
that accompany hypercarbia in this species arise from branchial receptors that
are present on more than just the first gill arch. In the only other studies
to utilise denervation techniques to identify branchial CO2
chemoreceptors (Burleson and Smatresk,
2000
; McKendry et al.,
2001
), the gills were totally denervated and thus it was not
possible to ascribe any preferential role to the first gill arch.
In the present study, both the bradycardia and the increase in ventilation amplitude caused by hypercarbia were initiated predominantly by receptors confined to the first gill arch. A shallow, yet statistically significant, positive correlation between PWCO2 and ventilation amplitude was observed in fish previously subjected to extirpation of the first gill arch. This finding indicates the involvement, albeit limited, of a population of CO2 receptors that are not specifically confined to the first arch. Upon examining the correlations between PWCO2 and ventilation amplitude (Fig. 2), it would appear that the first-gill-arch receptors are particularly important in mediating the ventilatory adjustments at relatively low levels of PWCO2 (e.g. <3 mmHg). Indeed, the ventilatory responses to higher levels of CO2 (>3 mmHg) appear to be similar in the intact and extirpated fish. Similarly, a shallow negative correlation was observed between PWCO2 and fH in extirpated fish (Fig. 3). Because this response was unaltered by atropine, it probably reflects a direct effect of CO2 on the heart rather than the presence of additional chemosensory sites for CO2. Alternatively, the bradycardia could reflect a loss of sympathetic neuronal tone to the heart that could not be overcome by increased humoral sympathetic stimulation (a consequence of the elevated plasma catecholamine levels).
Unlike in previous studies (Sundin et
al., 2000; Reid et al.,
2000
), the present study included additional experiments designed
to discern between external and internal orientation of the branchial
CO2 receptors. To preferentially stimulate presumptive external
receptors, a bolus of CO2-enriched water was injected into the
buccal cavity, whereas preferential stimulation of presumptive internal
receptors was achieved by injecting CO2-enriched saline into the
caudal vein. The interpretation of data from such experiments, however, is not
totally straightforward because the injection of CO2-enriched water
over the external surface of the gills would lead to some entry of
CO2 into the fish and thus cause the possible stimulation of both
external and internal chemoreceptors. Similarly, the injection of
CO2-enriched saline into the circulation could potentially activate
both internal and external receptors because of additional excretion of
CO2 into the ventilatory water. Despite the improbability of
exclusively stimulating a single population of receptors (external or
internal), it is likely that preferential stimulation of receptor populations
did occur in the present study. In other words, the extent of activation of
putative internal receptors would be trivial during external injections in
comparison with internal injections and vice versa.
The results clearly revealed the presence of external receptors linked to
bradycardia, increased systemic resistance, elevated ventilation amplitude and
catecholamine release. The external receptors linked to the cardiac and
ventilation responses were confined to the first gill arch, whereas the
receptors linked to resistance/pressure changes and catecholamine secretion
were more widely distributed amongst all the gill arches and/or present on
other external surfaces within the orobranchial cavity. The link between
activation of external CO2 chemoreceptors and elevation of plasma
catecholamine levels is particularly interesting considering current models
for catecholamine secretion in fish contend that the effects of CO2
(at least in part) are indirectly mediated by an impairment of blood
O2 transport (Reid et al.,
1998). While we cannot resolve the relative importance of the
direct and indirect actions of CO2 on catecholamine secretion
during hypercarbia, the potential for external CO2 receptors to
contribute directly to catecholamine secretion should be incorporated into
future models. The evidence for the notion that CO2 cannot directly
stimulate catecholamine secretion was obtained in experiments that compared
responses of trout to hypercarbia under normoxic or hyperoxic conditions
(Perry et al., 1989
). Because
hyperoxia prevented both the lowering of arterial O2 content and
catecholamine release during hypercarbia, it was argued that hypercarbia,
itself, could not be a specific stimulus. In the light of the present results,
however, an alternative explanation is that hyperoxia caused a blunting of the
response of the CO2 chemoreceptors to hypercarbia.
Apart from a slight bradycardia, there were no specific effects of
injecting CO2 internally on cardiorespiratory function or plasma
catecholamine levels. These results reaffirm the conclusions of previous
studies that externally oriented chemoreceptors responding to changes in the
PCO2 of the ambient water are largely
responsible for initiating the reflex responses to hypercarbia in trout
(McKendry and Perry, 2001) and
dogfish (Perry and McKendry,
2001
). This differs from the situation for O2
chemoreceptors, where separate populations of external and internal receptors
are thought to play specific roles in mediating ventilatory and cardiac
responses to altered ambient O2 levels. For example, it is believed
that external receptors preferentially confined to the first gill arch are
linked to cardiovascular and ventilatory reflexes, whereas more broadly
distributed internal receptors are linked to ventilatory reflexes
(Burleson et al., 1992
).
Removal of the first gill arch, in the absence of any other treatment, resulted in bradycardia and a decrease in breathing frequency. These results indicate that there may be tonic neuronal output originating from the first gill arch that serves to elevate heart rate and breathing frequency under resting conditions.
The branchial O2 chemoreceptors are believed to be phylogenetic
antecedents of the mammalian carotid body chemoreceptors
(Fritsche and Nilsson, 1993).
While it is known that the same carotid body chemoreceptors respond to
alterations in both PO2 and
PCO2
(O'Regan and Majcherczyk,
1982
), the response modalities of the branchial chemoreceptors are
uncertain. Clearly, there are receptors associated with the gill that respond
to changes in PO2 and
PCO2, but whether the same receptor responds to
both stimuli has not yet been established. While we cannot exclude the
presence of a class of receptor that responds to both O2 and
CO2, a comparison of the results of the present study (focusing on
CO2) with previous studies (focusing on O2) does provide
evidence for separate populations of O2- and CO2-sensing
receptors. For example, the internal gill receptors (which are not confined to
the first gill arch) linked to hypoxic hyperventilation
(Fritsche and Nilsson, 1993
)
appear to be insensitive to CO2 given (i) that
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Acknowledgments |
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