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First published online November 19, 2007
Journal of Experimental Biology 210, 4224-4232 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009266
The autonomic control and functional significance of the changes in heart rate associated with air breathing in the jeju, Hoplerythrinus unitaeniatus
1 Institut des Sciences de l'Evolution de Montpellier, UMR 5554
CNRS-Université Montpellier II, Station Méditerranéenne
de l'Environnement Littoral, 1 quai de la Daurade, 34200 Sète,
France
2 School of Integrative Biology, University of Queensland, Brisbane, QL
4072, Australia
3 School of Biosciences, University of Birmingham, Birmingham, B15 2TT,
UK
4 Department of Physiological Sciences, Federal University of São
Carlos, São Carlos, Brazil
5 Departamento de Zoologia, Centro de Aquicultura, UNESP, Rio Claro,
São Paulo, Brazil
* Author for correspondence (e-mail: david.mckenzie{at}univ-montp2.fr)
Accepted 19 September 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: air breathing, heart rate variability, teleost
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Graham et al., 1995;
Graham, 1997). Expiration is
typically associated with a bradycardia, followed by tachycardia upon
inspiration. In the swamp eel, Synbranchus marmoratus, and the South
American lungfish, Lepidosiren paradoxa, inspiration tachycardia is
associated with large increases in cardiac output and increased perfusion of
the air-breathing organ (ABO) (Johansen,
1966; Axelsson et al.,
1989; Skals et al.,
2006). There is some evidence to indicate that these
respiration-related variations in fH are under autonomic
control, in particular of inhibitory vagal cholinergic tone
(Axelsson et al., 1989;
Graham et al., 1995), and it
has been proposed that their role is to facilitate O2 uptake by air
breathing (Johansen, 1966;
Graham et al., 1995;
Skals et al., 2006).
Although air-breathing frequency is discontinuous and arrhythmic in fish
(Randall et al., 1981;
Graham, 1997), Graham et al.
(Graham et al., 1995) proposed
that the variations in fH were a homologue of respiratory
sinus arrhythmia (RSA), the cyclical variations in fH that
accompany the continuous rhythmic breathing of mammals. In mammalian RSA,
fH varies with the ventilation cycle because activity in
preganglionic neurones is inhibited during inspiration so that inhibitory
parasympathetic vagal tone on the heart is diminished and
fH rises. Parasympathetic tone is subsequently
disinhibited, producing a bradycardia on expiration
(Jordan and Spyer, 1987;
Taylor et al., 1999). It is
thought that these changes in vagal tone improve the efficiency of pulmonary
gas exchange by matching perfusion to ventilation within each breathing cycle
(Giardino et al., 2003).
How and when RSA might have evolved in vertebrates remains a topic of some
speculation (Porges, 1995;
Taylor et al., 1999;
Campbell et al., 2005;
Campbell et al., 2006a).
Indeed, there is a major difference in the association between heart rate
(fH) and ventilation rate (fV) between
fish that breathe continuously in water and mammals that do so in air. In
mammals, the rate association
fV<fH/2 must occur for the
development of the classic RSA oscillation effect, which alternates between
long and short heartbeat intervals. The presence of RSA in the instantaneous
electrocardiogram (ECG) in a continuous air breather can be revealed using a
mathematical technique known as power spectral analysis (PSA). If RSA is
present, the PSA output spectrum reveals distinct fundamental components at
the frequency of the ventilation cycle
(Akselrod et al., 1981;
Campbell et al., 2006a). In
fish, fV is almost always greater than half the heart rate
(fV>fH/2) and therefore the
sequence of cardiac intervals cannot be modulated by respiratory activity in
the classic RSA pattern (Zweiner et al.,
1995; Campbell et al.,
2006a). The PSA spectrum of the heart rate variability (HRV)
signal from water-breathing fish does not produce a fundamental component at
the frequency of ventilation but, instead, shows a number of peaks scattered
systematically through the spectral bandwidth, all at frequencies lower than
fV. These peaks cannot be considered to reflect RSA in
water-breathing fish but, nonetheless, they exhibit an association with shifts
in the length of each ventilation cycle, and a causal link between HRV and
ventilation can be revealed (Campbell et
al., 2005; Campbell et al.,
2006a; Campbell and Egginton,
2007).
Pharmacological parasympathetic blockade abolishes the PSA peaks in the
spectra of mammals, reptiles and water-breathing fish
(Medigue et al., 2001;
Campbell et al., 2004;
Campbell et al., 2006b). This
demonstrates that respiration-related modulation of activity at the sinoatrial
node, exerted via the parasympathetic vagus, is an essential component of HRV
in all animals examined to date (Medigue
et al., 2001; Campbell et al.,
2004; Campbell et al.,
2006b). Thus, although the control of cardio-respiratory coupling
events is still not completely understood in water-breathing fish, there does
appear to be some commonality in the autonomic control of HRV between animals
that breathe water and those that breathe air. Fish that respire in both air
and water offer the opportunity to examine these cardio-respiratory coupling
events in a single animal, and to determine the importance of each for
effective oxygen extraction. This may uncover the mechanisms of
cardio-respiratory synchronization that underlie the switch from water to air
breathing. Despite the ubiquitous occurrence of variations in
fH associated with air breathing in fish
(Randall et al., 1981;
Graham et al., 1995;
Graham, 1997), and its
qualitative similarity with the RSA of mammals, the relative roles of
inhibitory cholinergic versus excitatory adrenergic inputs in the
generation of HRV have not been described for any species.
The jeju, Hoplerythrinus unitaeniatus, is a facultative air
breather that uses a modified swimbladder as an ABO and which exhibits the
`typical' variations in fH during air breathing
(Farrell, 1978). In the
current study, we measured instantaneous beat-to-beat fH
from the ECG of jeju exposed either to normoxia or to deep aquatic hypoxia
(water PO2=1 kPa), and then used PSA to examine
patterns of HRV as a function of the prevailing frequencies of gill
ventilation (fV) and air breathing
(fAB). Pharmacological blockade was then used to
investigate the roles of adrenergic and cholinergic inputs in generating HRV,
and the relationship with bimodal ventilation patterns. Given the proposal
that the role of the HRV is to facilitate O2 uptake by air
breathing (Johansen, 1966;
Graham et al., 1995;
Skals et al., 2006), we
investigated the hypothesis that pharmacological abolition of HRV would reduce
the efficacy with which air breathing sustained routine metabolic rate in deep
hypoxia.
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Materials and methods |
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Surgery
Jeju were anaesthetized in tricaine methane sulphonate (MS-222, 0.3 mg
l–1), and placed on their side on an operating table with
their gills irrigated with an aerated solution of MS-222 at 0.1 mg
l–1. ECG recording electrodes (7-strand Teflon-coated wire,
length 40 cm, diameter 0.2 mm; A-M Systems Inc., Carlsborg, CT, USA) were
hooked into the end of a 24 G hypodermic needle and inserted through the
opercular septum at the base of the left 4th gill arch. The wires were placed
20 mm apart and advanced 4 mm through the septum; care was taken to ensure
that the pericardial membrane was not pierced. The trailing wire was attached
by a single suture to the flank of the fish just dorsal to the opercular flap.
A cannula (PE10 Intramedic, Clay Adams, Parsipany, NJ, USA) filled with
heparinized saline (10 i.u. ml–1 sodium heparin in 9 g
l–1 NaCl) was then inserted through a small puncture wound
(23 G needle) made just behind the left pectoral fin, into the peritoneal
cavity of the fish, and sutured to the body wall at the point of exit. This
cannula and the ECG wires were then sutured together to the back of the fish,
just rostral to the dorsal fin. Fish were allowed to recover in aerated water
at 26°C for at least 24 h prior to placement in the respirometry chamber.
The cannula was flushed gently with heparinized saline at 24 h recovery.
Respiratory metabolism and air-breathing behaviour
The instrumented jeju were transferred into clear plastic respirometry
chambers (volume 3 l) at approximately 19:00 h and allowed to recover and
acclimate overnight (at least 14 h) prior to experimentation. The ECG wires
and peritoneal cannula were led out of a small hole in the opaque plastic lid
of the chamber, so that they could be manipulated without disturbing the fish.
The respirometer was maintained at 26°C, by partial immersion in a large
outer plastic reservoir tank (volume 50 l) of aerated water. Instantaneous
O2 uptake from the water (MwO2, in
mmol O2 kg–1 h–1) was measured by
intermittent stop-flow respirometry
(Steffensen, 1989) as
described in detail previously (McKenzie
et al., 2007). Water O2 partial pressures
(PwO2) were measured with an oxygen electrode
(Radiometer E5046; Radiometer A/S, Brønshøj, Denmark) and
associated oxygen meter (Model 781, Strathkelvin Instruments, Glasgow, UK).
The output was relayed to an automated control and data acquisition system
(LoliDAQ, Loligo Systems ApS, Hobro, Denmark) with associated software
(LoliResp, Loligo Systems ApS), which calculated
MwO2 from 10 min cycles of water recirculation
through the respirometer chamber, interrupted by a flushing cycle, both
generated by submerged water pumps (Eheim Gmbh & Co KG, Deizisan,
Germany).
The water in the outer tank was level with the lid of the respirometry
chamber, and this was fitted with a dome-shaped airspace (volume 150 ml) that
allowed the animal to surface and gulp air. The dome had an aperture at its
apex that was sealed with a rubber bung during experiments, and the moist air
in the sealed space was drawn, by a peristaltic pump (MCP-E-60, Ismatec SA,
Labortechnik-Analytik, Glattbrugg, Switzerland) via gas-impermeable Tygon
tubing, past an O2 electrode (model 16-730 flow-through electrode;
Microelectrode Inc., Bedford, NH, USA) and then pushed back into the air dome.
The electrode was connected to an O2 meter (model OM4,
Microelectrode Inc.) and the signal from this was continuously displayed and
recorded on a PC with Logger Pro software (Vernier Software and Technology,
Beaverton, OR, USA), via a Lab Pro data collection device (Vernier Software
and Technology). Air breaths by the fish were visible as stepwise declines in
the PO2 signal from the air in the dome
(PaO2), which were completed in between 3 and 5
s and were confirmed visually (see below). Instantaneous O2 uptake
from the air (MaO2, in mmol O2
kg–1 h–1) was calculated from the rate of
decline in O2 in the airspace, as described in detail by McKenzie
and Randall (McKenzie and Randall,
1990). The decline in airspace PO2
following each air breath was so discrete and rapid that it was not necessary
to correct for potential gradual exchange of O2 between air and
hypoxic water (see below). The O2 in the airspace was replaced at
intervals by gently removing the bung and flushing the dome with an air-filled
syringe (volume 60 ml). Total oxygen uptake
(MtO2) was calculated by summing
MwO2 and
MaO2.
To minimize any disturbance to the fish, which might influence
air-breathing behaviour and therefore respiratory partitioning
(Shingles et al., 2005), the
whole setup was shielded from view behind sheets of cardboard on a large
wooden frame. A digital video camera filmed the behaviour of the fish through
the clear plastic fronts of the reservoir tank and respirometry chamber, with
the images displayed on a PC. The fish could also be observed directly through
a small hole cut into one of the cardboard sheets. The air breaths shown on
the video signal and PaO2 trace were used to
calculate air-breathing frequency (fAB, in breaths
h–1) and its reciprocal, the interbreath interval (IBI, in
min).
Electrocardiograms
The instantaneous ECG was recorded using a bioamplifier interfaced with a
digital recording system (PowerLab, ADInstruments, Oxford, UK). ECG was
sampled at 400 Hz and both the ECG and gill fV (opercular
movements) could be observed as different frequency components transposed onto
a single trace (see Campbell and Egginton,
2007). Bipolar ECG signals were recorded continuously immediately
after placement in the respirometer. When the fish took an air breath, this
was noticeable as a distinct artifact on the ECG trace. This was correlated
with the video image of the air-breathing behaviour and the sudden drop in
PO2 in the air dome.
Experimental protocol
Following overnight recovery, normoxic values for respiratory and cardiac
variables were collected on the undisturbed jeju for at least 1 h.
Subsequently, the water PO2 was reduced to
1±0.2 kPa by bubbling 100% N2 into the outer reservoir tank.
It took about 2 h 20 min for the PwO2 to
stabilize at this extreme degree of hypoxia, and all variables were measured
throughout this period. The fish were maintained at this hypoxic
PwO2 for 1 h and all variables were measured
continuously. While still hypoxic, the animals were then infused via their
peritoneal cannula with 1 ml kg–1 of 10–5
mol l–1 propranolol hydrochloride (Sigma-Aldrich, St Louis,
MO, USA) dissolved in saline (9 g l–1 NaCl) and all variables
were again measured for 1 h. Subsequently, also while still hypoxic, the
animals were infused with 1 ml kg–1 of a cocktail of
10–5 mol l–1 propranolol hydrochloride plus
10–5 mol l–1 atropine sulphate (Sigma)
dissolved in saline. All variables were again measured for 1 h and then the
animals were recovered to normoxia by bubbling air into the reservoir tank.
This required about 1 h, and then all variables were measured for at least 40
min in normoxia.
Supporting pharmacological studies
In order to investigate the effects on hypoxic HRV of reversing the order
of the pharmacological treatments, jeju (N=4) were exposed to deep
hypoxia, as described, and then treated with the same doses of drugs, but with
atropine sulphate given before propranolol hydrochloride. To ensure that the
doses of atropine and propranolol used in the study were effectively blocking
cholinergic and adrenergic control of the heart in the jeju, acetylcholine
chloride (10–5 mol l–1) and then
phenylephrine (1 ml kg–1 of 10–5 mol
l–1 solution) were infused via the cannulae 1 h after
infusion of the respective antagonists and resultant changes in ECG were
recorded. Oxygen uptake was not measured during these experiments.
Analysis of data
Respiratory metabolism and air-breathing behaviour
Oxygen uptake was measured for the last 40 min of each condition and mean
MwO2, MaO2 and
MtO2 were calculated. These data were then
compared between conditions by one-way analysis of variance (ANOVA) for
repeated measures. The percentage of MtO2 met
by either water or air breathing was also calculated and compared between
treatments by the same method, following arc-sine transformation of the data.
Air-breathing frequency and IBI were similarly calculated and compared between
treatments. In those cases where the groups failed normality
(Kolgorov–Smirnov test), a non-parametric ANOVA for repeated measures
based upon ranks was applied.
Calculations of autonomic tonus on the heart
To calculate the relative cholinergic (Chol, %) and adrenergic (Adr, %)
tone the following equations were used, modified from Campbell et al.
(Campbell et al., 2004):
 | (1) |
 | (2) |
;
Campbell et al., 2006a). The
resultant output is plotted graphically, where oscillations in
fH will appear at their relative frequencies in the power
spectrum. |
Results |
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The β-adrenergic receptor blockade with propranolol caused MwO2 to fall to zero but had no significant effects on MaO2 or MtO2. The drop in MwO2 was associated with a significant decline in fV (Table 1). It was also associated with a significant increase in the percentage of metabolism met by air breathing when compared with the untreated hypoxic fish, although there was no significant effect upon fAB or IBI (Table 1). When subsequently given a total autonomic blockade by treatment with the atropine and propranolol cocktail, MwO2 and fV returned to the rate measured in hypoxia prior to β-adrenergic receptor blockade (Table 1). There was, however, no significant effect of total blockade upon MaO2, MtO2 or fAB (Table 1). Finally, recovery to normoxia was associated with a significant increase in MwO2, although there was no change in fV. There was, however, a decline in MaO2 and fAB (Table 1). The slight elevation of mean MtO2 that is apparent during recovery (Fig. 1, Table 1) was not statistically significant but was associated with a visible increase in the activity level of the fish in their respirometers, as observed on the video recording.
Heart rate, heart rate variability and its autonomic regulation
Overall, mean fH was not significantly different in
normoxic compared with hypoxic water. However, HRV was greatly increased in
hypoxia, as a result of the pronounced increase in fAB.
Prior to each AB, there was a significant decline (18–21%) in mean
fH, and after inhalation of air into the modified
swimbladder fH rose by 81.5%
(Table 2,
Fig. 2A). The infusion of
propranolol reduced overall fH. The fH
prior to each AB was suppressed to a greater extent (24.3%) than the
fH following the AB (10.4%), and therefore adrenergic
receptor blockade had the effect of causing a larger disparity in
fH prior to versus following each AB
(Table 2,
Fig. 2B). The second effect of
adrenergic receptor blockade was to increase the time taken for
fH to return to a steady state after each AB.
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The infusion of the β-muscarinic acetylcholine receptor blocker atropine significantly increased fH and abolished all of the marked changes in fH that accompanied each AB (Fig. 2C). It also abolished all the other HRV components.
Calculation of relative tonus using Eqns 1 and 2 showed that adrenergic tonus was 75.51% before the AB and 47.28% after the AB, and cholinergic tonus was 304.3% before and 81.5% after the AB.
Fig. 3 shows representative results of PSA on R–R intervals of a jeju in normoxia then hypoxia with the pharmacological treatments. In normoxia, when the fish did not exhibit air breathing, the fH showed high frequency beat-to-beat variation (Fig. 3Ai). The R–R intervals formed two discrete groups in period length with centre frequencies of 1650 and 2150 ms (Fig. 3Aii). The switch between each R–R interval length was oscillatory in nature and the frequency of these oscillations was observed as fundamental components in the power spectrum between 0.147 and 0.189 Hz (Fig. 3Aiii). Calculated in the time domain (1/Hz) the length of each of these oscillations was between 6.8 and 5.2 s, and corresponds to a beat frequency of two to three heartbeats.
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A major effect of propranolol was to abolish the oscillation in short-term beat-to-beat variability observed in non-blockaded fish. Although short-term HRV occurred it did not form distinct groups and the R–R intervals were instead spread between 1250 and 2400 ms with no centre frequencies (Fig. 3Cii). The loss of the oscillatory component was confirmed by the absence of discrete high frequency components in the power spectrum (Fig. 3Ciii). The further infusion of atropine abolished all HRV, and with total blockade the heart beat at a very steady rate and did not vary at all with the AB (Fig. 3Di,ii) and, therefore, no components whatsoever were observed in the power spectrum. (Fig. 3Diii).
Although the HRV results are only provided for a single representative jeju, the patterns described were similar for all individuals, with the mean rate changes in fH shown in Table 2 and Fig. 2. Reversing the order of the autonomic blockades, i.e. atropine prior to propranolol, did not change the resulting total blockade effect, although fH changes around the AB induced by propranolol could not be observed if atropine was infused first. When acetylcholine and phenylephidrine were infused 1 h after blockade, they had no significant effect on fH, which confirmed that the doses of propranolol and atropine applied had caused total effective blockade of adrenergic and β-muscarinic receptors (data not shown).
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Discussion |
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Video recordings of un-instrumented jeju, made over 24 h in the same
respirometer chambers as used in the current study, revealed that they did not
air breathe any more frequently in normoxia than the instrumented animals
described here (D.J.M., unpublished observations), indicating that
air-breathing behaviour had not been influenced by the presence of the ECG
wires and peritoneal catheter. The almost total absence of air breathing in
aquatic normoxia in the current study is consistent with other reports for
this species at a similar temperature
(Oliveira et al., 2004;
Perry et al., 2004), but the
associated minimal proportion of MtO2 that was
met by air breathing differs from that reported by Randall et al.
(Randall et al., 1978), where
MaO2 represented up to 20% of routine metabolic
rate in normoxia. When the jeju was in normoxia and air breathing very
infrequently, mean fV was slightly more than twice
fH. A situation where
fV>fH/2 is typical of unimodal
water-breathing fish species (Stevens and
Randall, 1967; Campbell et al.,
2004; Campbell et al.,
2005; Campbell et al.,
2006a) and the sequence of cardiac intervals cannot be modulated
by respiratory activity in the classic RSA pattern
(Zweiner et al., 1995;
Campbell et al., 2006a).
Indeed, in normoxia the PSA spectrum of HRV in the jeju was qualitatively
similar to that of unimodal water-breathing fish, with a number of peaks
scattered systematically throughout the spectral bandwidth, all at frequencies
lower than fV (Campbell
et al., 2005; Campbell et al.,
2006a).
When exposed to deep aquatic hypoxia, the jeju was able to maintain aerobic
metabolism at routine levels through a large increase in
fAB. This increase was presumably a result of the
stimulation of oxygen-sensitive chemoreceptors
(Smatresk et al., 1986;
McKenzie et al., 1991), and
the PwO2 threshold for the increase in
MaO2 coincides well with the hypoxic
PwO2 at which previous studies have noted a
stimulation of fAB in this species
(Oliveira et al., 2004;
Perry et al., 2004). Perry et
al. (Perry et al., 2004)
exposed jeju to a level of deep aquatic hypoxia similar to the current study
(PwO2 
1.3 kPa) and demonstrated that air
breathing allowed them to maintain arterial blood O2 content
unchanged from normoxia, indicating that they were not experiencing systemic
hypoxia. It is interesting that the jeju did not exhibit any significant
changes in fV in hypoxia. In unimodal water-breathing
fish, hypoxia elicits gill hyperventilation via a chemoreceptor-driven reflex
(Burleson et al., 1992) but
air-breathing fish exhibit a diversity in gill ventilatory responses that
reflects the complex nature of physiological strategies for bimodal
respiration (Graham, 1997),
with some species showing a reflex decrease
(Smatresk et al., 1986) but
others a reflex increase (McKenzie et al.,
1991) in fV. Perry et al.
(Perry et al., 2004) reported
that the in vivo P50 for whole blood of this species was
approximately 1 kPa (7.7 mmHg). Such a high affinity Hb might explain why the
jeju in the current study managed to retain net O2 uptake from
water in very deep hypoxia. Additionally, the jeju did not show any change in
mean fH in hypoxia, with no evidence of the hypoxic
bradycardia reported by Oliveira et al.
(Oliveira et al., 2004). The
reason for this disparity in response is not clear; Farrell
(Farrell, 2007) proposed that
air-breathing fish should not exhibit hypoxic bradycardia if their
air-breathing strategy allowed them to maintain O2 delivery to the
myocardium, but this remains to be tested.
The typical cycling of bradycardia then tachycardia with each AB cycle has
been reported previously in H. unitaeniatus
(Farrell, 1978) and, in the
current study, this was associated with a significant increase in HRV in
hypoxia. The quantitative relationship between fAB and
fH was in a range similar to that of animals which only
utilize air breathing (Akselrod et al.,
1981; Campbell et al.,
2006a) and, indeed, a relationship where
fAB<fH/2 clearly prevailed. This
was associated with a pronounced fundamental component in the power spectrum
that was coherent with the IBI for air breathing. For the jeju, therefore, the
tachycardia and marked decline in HRV during inspiration may have reflected an
inhibition of preganglionic neurones (e.g. the baroreflex), while the
bradycardia and associated increase in HRV on expiration (immediately prior to
surfacing) may have reflected disinhibition of cardiac vagal tone, in a manner
similar to what is known for mammals
(Jordan and Spyer, 1987;
Taylor et al., 1999). However,
the overall HRV pattern observed in the jeju was quite different from the RSA
effect as documented for mammals (Akselrod
et al., 1981; Giardino et al.,
2003) and recently in a reptile
(Campbell et al., 2006b). This
is because, although there were marked changes in fH
directly associated with the irregular AB events, in the intervals between
each event a situation where
fV>fH/2 prevailed, and the HRV
pattern was the same as had been observed in the fish relying exclusively upon
gill ventilation in normoxia. Indeed, the PSA demonstrated that the jeju in
hypoxia still exhibited the same higher frequency peaks that had been observed
scattered through the spectrum in normoxia. These peaks are, therefore,
entirely independent of any effects of air breathing upon
fH.
The effects of autonomic blockade on air breathing have never been
investigated in fish; the absence of any effect of propranolol on
fAB indicates that β-adrenergic receptors play no
role in regulating these reflexes in hypoxia. On the other hand, the
significant decline in fV following treatment with
propranolol has been reported in other fish
(McKenzie et al., 1995). The
significant decrease in MwO2 following
β-adrenergic receptor blockade may have reflected this inhibition of gill
ventilation. It is particularly interesting, indeed, that the propranolol
abolished the discrete higher frequency components of the HRV signal, as these
are qualitatively similar to spectral components that have been causally
related to gill ventilation in unimodal water-breathing fish
(Campbell et al., 2005;
Campbell et al., 2006a). It is
tempting to speculate that there may be a causal link between these components
of the spectrum and gill ventilation patterns in the jeju, although this
clearly requires experimental verification. In any case, it is unusual that
the adrenergic system should play a role in the high frequency beat-to-beat
oscillation of fH
(Jordan and Spyer, 1987;
Taylor et al., 1999).
Respiratory sinus arrhythmias are classed as high frequency oscillations
caused by vagal stimulation of the sinus node, with adrenergic tonus being
responsible only for low and mid-frequency changes in fH
(Jordan and Spyer, 1987;
Taylor et al., 1999). The
results of the cholinergic blockade revealed that inhibitory vagal tone was
indeed responsible for the greatest proportion of the HRV in the jeju, as is
the case for mammals and fish (Jordan and
Spyer, 1987; Taylor et al.,
1999; Campbell et al.,
2004; Campbell et al.,
2005), and that this inhibitory tonus modulated the greatest part
of the changes in fH around each AB event. Vagal tone in
the jeju was very high by comparison with most unimodal water-breathing fish
species (Altimiras et al.,
1997). The jeju, however, exhibited a very unusual pattern in
autonomic regulation because the adrenergic and cholinergic components
appeared to work in concert rather than antagonistically. That is, the
bradycardia prior to each AB was associated with a pronounced increase in HRV
that was caused by a simultaneous rise in both adrenergic and cholinergic
tone. Following the AB, the tachycardia was associated with a drop in
cholinergic and adrenergic tone and a severe reduction in HRV. In all fish
studied to date, and in the vast majority of all other vertebrates, the
parasympathetic and sympathetic branches of the autonomic nervous system work
reciprocally, and thus their effects are compounded
(Taylor et al., 1999). The
only exception of which the authors are aware is the bearded lizard
(Pogona barbata) (Seebacher and
Franklin, 2001). It is not clear whether this apparently
paradoxical pattern of autonomic regulation in the jeju might also be found in
other fish species with bimodal respiration. Furthermore, given the existence
of this profound but unusual autonomic control of the heart in the jeju, and
its clear relationship with air breathing, it is perhaps somewhat surprising
that pharmacological blockade of all HRV had no effect whatsoever upon
fAB and the regulation of routine metabolism by air
breathing in deep hypoxia.
It is possible that the changes in fH that accompany
air breathing might facilitate oxygen uptake from the ABO under conditions
where metabolic demand is high, for example during aerobic exercise
(Farmer and Jackson, 1998).
There is also a large behavioural component to surfacing and gulping air, with
fear of predation being a significant factor that can influence patterns of
surfacing activity in air-breathing fish
(Smith and Kramer, 1986). Fear
of predation can also cause a reflex bradycardia in fish, and this can
influence the timing and intensity of cardiac chemoreflexes during surfacing
behaviours (Shingles et al.,
2005). Thus, it is conceivable that some element of the changes in
fH during air breathing might reflect higher order
behavioural inputs linked with approaching the water surface.
In conclusion, the jeju exhibits HRV patterns that are qualitatively
similar to those of both water-breathing and air-breathing vertebrates, and
these patterns may be controlled independently of each other. The expiration
bradycardia and the inspiration tachycardia with each AB are qualitatively
similar to mammalian RSA, but after each AB the fish quickly return to the HRV
pattern of a water-breathing fish. The adrenergic and cholinergic tone rose
and fell together around each AB event, which is very unusual and appears
paradoxical. Nonetheless, pharmacological abolition of all these HRV patterns
was without effect upon fAB or the efficacy with which the
jeju regulated metabolism by air breathing in deep hypoxia. This may indicate
that the HRV patterns associated with air breathing do not function to
facilitate O2 uptake from the air-breathing organ. It should be
kept in mind, however, that it is very difficult to detect the role of RSA in
optimizing gas exchange in mammals
(Giardino et al., 2003), and
so this is an interesting area for future research in air-breathing fish.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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