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1 Department of Biological Sciences, University of North Texas, Denton, Texas 76201; and 2 Danish Center for Respiratory Adaptation, Department of Zoophysiology, University of Aarhus, Aarhus 8000, Denmark
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Adrenergic and cholinergic tone on the cardiovascular system of
embryonic chickens was determined during days 12,
15, 19, 20, and 21 of
development. Administration of the muscarinic antagonist atropine (1 mg/kg) resulted in no significant change in heart rate or arterial
pressure at any developmental age. In addition, the general
cardiovascular depressive effects of hypoxia were unaltered by
pretreatment with atropine. In addition, the ganglionic blocking agent
hexamethonium (25 mg/kg) did not induce changes in heart rate. The
-adrenergic antagonist propranolol (3 mg/kg) induced a bradycardia
of similar magnitude on all days studied, with a transient hypertensive
action on days 19-20, indicating the existence of an
important cardiac and vascular -adrenergic tone. Injections of the
-adrenergic antagonists prazosin or phentolamine (1 mg/kg) reduced
arterial pressure significantly on all days of incubation studied.
Collectively, the data indicate that embryonic chickens rely primarily
on adrenergic control of cardiovascular function, with no contribution
from the parasympathetic nervous system.
vagal tone; adrenergic tone; cardiovascular regulation
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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EMBRYONIC CHICKENS have long been used for the study and understanding of cardiovascular function as well as regulation during vertebrate ontogeny. Several studies have focused on the onset of neurohumoral cardiac regulation, but little is known of its functional significance during embryonic development. In addition, neurohumoral control of peripheral vascular beds, which is essential for blood pressure regulation, has been only poorly characterized.
Despite this limited knowledge, several morphological and physiological traits have been identified in developing chickens. Cardiac muscarinic and adrenergic receptors are present in embryonic chickens during the first quarter of incubation (3). In addition, the anabolic and catabolic enzymes of the primary autonomic neurotransmitters (acetylcholine and norepinephrine) are also present during early development (14, 34). Prior research using field stimulation methods established that autonomic efferents are capable of releasing acetylcholine from cholinergic fibers on day 12, whereas sympathetic release of norepinephrine is possible on day 21 of incubation (23). These data demonstrate the functional integrity of autonomic efferent pathways; however, they do not confirm the presence of a tonic cardiovascular regulation in embryonic chickens.
In embryonic chickens a functional cholinergic tone on the cardiovascular system would require the maturation of both afferent and central elements, which may not occur until later in development. Similarly, a functional adrenergic tone would require maturation of afferent and central elements of the sympathetic system; however, additional adrenergic tone may originate from blood-borne catecholamines. Circumstantial evidence suggests that a tonic regulation occurs in embryonic chickens (30). However, to our knowledge, a systematic study encompassing different developmental days with an appropriate statistical treatment of the data has not been completed.
Thus the present study was undertaken to further our understanding of
neurohumoral cardiovascular regulation in developing avian embryos.
Antagonists of the common receptors involved in cardiovascular
regulation were administered throughout ontogeny (i.e., muscarinic and
- and -adrenergic receptor antagonists) to address this issue. In
addition, experiments were conducted with ganglionic blocking agents as
well as hypoxic stress to further address the role of vagal function in
cardiovascular control. Finally, given the potential for catecholamines
originating from nonneural sources to target adrenoreceptors, a
simultaneous determination of circulating plasma levels of
catecholamines was conducted.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Experimental animals. Experiments were carried out in two series conducted over the period from November 1998 to March 1999. Series I was conducted on chicken eggs of the Plymouth Russ208 strain purchased from Fællesrugeriet (Randers, Denmark) at the University of Aarhus. Series II was conducted on chicken eggs of the White Leghorn strain purchased from the Texas A&M University poultry farm at the University of North Texas. On arrival eggs were placed in incubation at 38°C and 60-70% relative humidity and were turned automatically every 3 h. Embryos incubated for 12, 15, 19, 20, and 21 days of a 21-day incubation period were studied. The 20-day-old embryos were defined as internally pipped embryos, as verified by candling, and 21-day-old embryos were defined as externally pipped embryos. The work in Denmark was carried out under University of Aarhus permit number 1997-101-112. The work completed in the US was carried out under University of North Texas animal protocol UNT-00-01.
Measurement of blood pressure and heart rate. At selected developmental ages, eggs were removed from the incubator, candled to trace the major chorioallantoic arteries with a soft pencil, and placed in a vermiculite bath (38°C). A chorioallantoic membrane (CAM) artery was exposed by removal of a small portion of eggshell. The smallest branching vessel was occlusively cannulated with a polyethylene catheter (PE-90, Clay-Adams) with the tip heat-pulled to an outer diameter of ~0.5 mm under a dissection microscope. Silk suture was used to secure the catheter to the vessel after careful alignment of the two, and the catheter was glued to the eggshell with cyanoacrylic glue (VetBond 3M). On completion of the surgical procedures, each egg was returned to the experimental chamber. In series I, the experimental chamber consisted of a 500-ml stainless steel water-jacketed trough fitted with a lid containing four circular openings. Eggs were placed blunt end up on a small amount of vermiculite within the openings, which resulted in the egg resting within the trough below the level of the lid. Each opening was then covered with a 50-ml dome containing a 1-cm opening to allow passage of the arterial catheter as well as passive circulation of room air. In series II, the experimental chamber was modified to allow a precise control of the gas environment of the embryos. The glass water-jacketed chamber (300 ml) was fitted with a glass lid with three holes allowing the flushing of different gas mixtures as well as the connection of the catheter to blood pressure transducers. With this system each chamber was continually flushed with water-saturated room air that had been circulated through a heated sand bath at 37°C. Oxygen content (% O2) in the chamber was continuously monitored with an oxygen analyzer (model S 3A-1, Applied Instruments).
Blood pressure traces were obtained via fluid-filled catheters connected to Statham pressure transducers (P23) that were calibrated against a static water column. The transducer was connected to a Beckman recorder (R511A) for proper amplification of the signal before being sampled at 500 Hz by a computer via a Data Translation card (DT2801A) and LabView custom-made acquisition software. Heart rate (fH) was obtained from the pressure signal. Zero-pressure reference for the system was completed as previously described (1). Briefly, a nominal "zero point" was set at the top edge of the eggshell for the entire study. Once the experiment was completed, the embryo was euthanized and quickly frozen at
20°C. After this procedure, the egg was cut along the
longitudinal axis to determine the relative position of the embryo and
the heart in relation to the top of the eggshell. An offset correction
of all pressure data was then conducted to determine pressure on each
day of study.
Experimental protocol.
In each series the experiment included a sequential arterial injection
of antagonists of the main receptors involved in adult vertebrate
cardiovascular control. These blocking agents included atropine (1 mg/kg, Sigma) to characterize vagal tone, propranolol (3 mg/kg, Sigma)
to characterize -adrenergic tone, and prazosin or phentolamine (1 mg/kg for both drugs, Sigma) to characterize the role of
1- and 2-adrenergic receptors on the
developing cardiovascular system. The efficacy of the antagonists was
tested in preliminary experiments, because the antagonist blocked the effects of a subsequent injection of the agonist (Fig.
1). Injection volumes were normalized for
each embryonic age to 5% of the total blood volume based on literature
data (Table 1; Ref. 25). Each dose was calculated taking into account the total mass of living tissue
in the egg (including total embryonic wet mass as well as the total
mass of the egg membranes; Ref. 25). Special care was taken to avoid
large volumes of dead space in injection lines with each drug
administration.
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70°C until analysis was carried out (within 1 mo). HPLC analysis of plasma catecholamines was carried out as
previously described (9).
Two additional experiments were carried out as part of series
II in an attempt to further assess the tonic role of the vagus nerve in cardiac control. The first experiment involved an exposure to
10% O2 for 5 min, followed by an injection of atropine (1 mg/kg), stabilization for 20 min, and reexposure to 10%
O2. Hypoxic gas concentrations were achieved by volumetric
mixing of nitrogen and room air.
The second experiment consisted of the injection of hexamethonium
chloride (25 mg/kg, Sigma), a ganglionic blocking agent. This dosage
was within the range previously used for assessment of ganglionic
activity in fetal and newborn mammals (1-25 mg/kg; Refs. 6, 15,
22, 27). In each experiment, six embryos at each incubation age were
used. Total protocol length in each series was 1 h.
Statistics.
Mann-Whitney U and Wilcoxon nonparametric tests were used to
assess statistical differences between chicken strains (series I and series II), developmental days, and treatments
(hypoxia and drug administration: atropine, propranolol, -blocker,
and hexamethonium). Because repeated tests were carried out, thereby using the same data more than once, the fiduciary limit
(P = 0.05) was corrected according to the number of
times each data set was used, commonly three or four times because the
tests between developmental days were restricted to adjacent days
(thereby comparing days 12-15,
15-19, 19-20, and
20-21). All data are presented as means ± SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Comparison of control values between experimental series.
The values obtained are in general agreement with prior research over
this period of chicken development (13, 17, 32). Mean
arterial pressure (MAP) rose in a similar manner (from 0.37 to 3.5 kPa)
in each series from day 12 to day 21 of
incubation (Fig. 2), with significant
differences between series on day 20 only. In addition,
fH on each day of incubation in each series showed no statistical difference (Fig. 2); therefore, the data from
both series were pooled for further analysis.
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Effects of cholinergic antagonists and hypoxia.
The muscarinic antagonist atropine did not significantly alter MAP or
fH on any developmental day studied, and the
ganglionic blocker hexamethonium did not significantly alter MAP or
fH in series II (Table
2). Similarly, the pronounced
cardiovascular changes caused by hypoxia were unaltered by atropine
treatment (Table 3); Fig.
3 presents the cardiovascular response to
hypoxia without atropine treatment. All these findings are
summarized in Table 3, which illustrates the predicted (as expected in
adult chickens) vs. observed responses to each manipulation used to induce a vagal response.
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Effects of adrenergic antagonists.
Propranolol injection caused a pronounced bradycardia (38 ± 3 beats/min) on all days studied, with a transient pressure effect on
days 19 and 20 (0.33 ± 0.04 kPa) of
incubation (Fig. 4, A and
B). This significant fH response to
-blockade changed in intensity with embryonic development (day
12 < day 15 = day 19 < day 20), as illustrated in Fig. 4B. Although
developmental changes in response intensity have not been tested
previously, all other cardiovascular responses are in agreement with
those of a prior study on embryonic chickens aged 12 to 21 days
(31).
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-adrenoceptor antagonists from each study series induced similar
cardiovascular responses despite their differing specificity for
1- and 2-receptors (Table
4). Given this result, statistical analysis was conducted on the pooled data from each series. In general,
-blockade resulted in a clear hypotensive bradycardia on all
incubation days tested, with the notable exception of day 21 (Fig. 5, A and B).
The extent of this response varied throughout development, with
pressure changes ranging from 0.15 ± 0.02 kPa to 1.27 ± 0.29 kPa (Fig. 5A) and a bradycardia ranging from 12 ± 2 to 55 ± 12 beats/min (Fig. 5B).
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Plasma levels of catecholamines during development.
The concentrations of norepinephrine, epinephrine, and dopamine showed
significant changes as embryonic maturation proceeded (Table
5). Norepinephrine levels peaked on
day 19 at 169.4 ± 52.0 ng/ml, a level significantly
higher than that on earlier days (P < 0.05).
Epinephrine exhibited a similar increase to 80.6 ± 23.2 ng/ml on
day 19, again significantly higher than that on earlier days
(P < 0.05). Finally, dopamine peaked at 9.1 ± 1.3 ng/ml on day 20, significantly higher than
that on earlier days (P < 0.05).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Tonic regulation of cardiovascular function during late development in embryonic chickens exhibits distinct attributes that differ from those present in hatchling as well as adult animals (28). This study has demonstrated that in embryonic chickens basal cardiovascular function is maintained primarily via tonic adrenoreceptor stimulation, whereas vagal tone remains absent.
Cardiac regulation: vagal and -adrenergic tones.
Field stimulation of embryonic atrial tissue has previously shown that
the release of acetylcholine from postganglionic synapses can occur as
early as day 12 of incubation in chickens (23). Thus day 12 has traditionally been thought to represent the
onset of parasympathetic regulation of the heart and, by extension, of
the cardiovascular system in embryonic chickens.
-adrenergic tone
that is important for the maintenance of basal chronotropic activity.
Although the heart rate response of embryonic chickens to -blockade
(26, 30) is similar to that of adults (cf. Ref. 4), the
participation of sympathetic efferents in cardiac regulation is
unlikely in embryos (12, 23). Therefore, the adrenergic tone is presumably related to the increasing levels of circulating catecholamines (Table 5). Further evidence is provided by the lack of
action of hexamethonium that, as previously indicated, blocks
postganglionic autonomic transmission.
The catecholamine levels reported here are consistently higher than
those determined in an earlier study (7) while being similar to those reported on days 19-21 in a second
study (33). Because blood was obtained by hemorrhage,
which can trigger the release of catecholamines (unpublished
observations), the plasma levels measured here may indicate the
capacity for release under cardiovascular stress rather than the
resting levels in the plasma. Regardless of the capacity for
catecholamine release into the plasma, embryonic chickens do not
exhibit a concomitant increase in cardiac reactivity to propranolol,
which might be instrumental in preventing a supramaximal stimulation of
the heart. Over the period of 17 to 19 days of incubation the pacemaker
tissue, as well as the ventricle, is subsensitive to catecholamines
(12, 20), probably because of the saturation of the
receptors, downregulation, or desensitization. The peak activity of
catechol-o-methyl transferase and monoamine oxidase
(catabolic enzymes responsible for the inactivation of catecholamines)
in cardiac tissue of chickens also occurs on days 19-20
(14). Collectively, these studies may explain the constant
cardiac response to propranolol in the presence of increasing plasma
catecholamines. Thus the experimental evidence indicates that humoral
catecholamines play a role in tonic cardiac regulation, although the
specific details on how this is achieved require further research.
Vascular regulation: - and -adrenergic tones.
Given that extraembryonic vascular beds lack autonomic innervation and
that the innervation of intraembryonic vasculature is nonfunctional,
vascular regulation during development must be based primarily on
humoral factors such as catecholamines.
- or -antagonist indicate a dependence on different populations of adrenergic receptors for vascular regulation. After propranolol injection, chicken embryos exhibited a clear hypertension on days 19 and 20 (26,
30), opposite to the hypotension occurring in adult chickens
(4, 17). These different pressure responses are likely
related to the presence of a chorioallantoic vascular bed in embryos, a
structure that has been suggested to be analogous to the mammalian
placenta (21). If the chorioallantoic vasculature has an
active population of -adrenergic receptors, as has been suggested
for the mammalian placenta (5), it could result in an
accentuated -adrenoreceptor vasodilation in embryonic chickens. Thus
the negative inotropic action, which typifies the adult cardiac
reaction to -blockade, may be masked by an overriding chorioallantoic vasoconstriction in embryonic chickens, resulting in
hypertension. Such a dilatory tone may have important consequences for
the regulation of blood oxygenation during chicken development.
In contrast to the primary cardiac actions of -antagonists,
injections of -antagonists revealed strong -adrenergic tone on
the vasculature (Fig. 5A). Prior studies showed similar
hypotensive results after -blockade in embryonic chickens from
day 6 to day 16 (18, 26, 30).
Qualitatively, results with either -blocking agent were similar,
suggesting that the 1-receptor is the primary -subunit responsible for maintaining vascular tone in embryonic chickens.
In addition to the vascular responses, -adrenergic blockade also had
a negative effect on cardiac activity. Given the action of phentolamine
on cardiac function in adult mammals, the possible contribution of
cardiac -adrenergic receptor blockade to the decrease in embryonic
heart rate must be acknowledged (8). However, it is
plausible that the negative chronotropic action of -blockade could
be secondary to the general vasodilation, resulting in a reduced venous
return to the heart caused by blood pooling in the extraembryonic
circulation. Determination of the changes in vascular resistance after
selective -blockade are needed to establish the origin of any
negative chronotropic action.
As illustrated in Fig. 5A, day 19 and
20 embryos exhibited the highest reactivity to -blockade
whereas day 21 embryos were unaffected by drug treatment.
This response indicates that, as previously suggested
(10), there is a dependence on -adrenergic tone to
maintain basal cardiovascular function that is maximal just before
internal pipping and lung ventilation. Similar results have been
obtained in fetal sheep, which show an increase in -adrenergic tone
with a magnitude that peaks at the end of gestation (2). Such a late gestational dependence on adrenergic receptors is essential
for the maintenance of fetal cardiovascular performance during the
asphyxia associated with parturition (16, 19). This
dependence then decreases dramatically in the neonate after parturition
and resumption of normoxic blood PO2 associated
with lung ventilation. An analogous event may explain the peak and subsequent drop in -adrenergic tone late in chicken ontogeny. As the
embryonic gas exchange organ regresses, an increased -adrenergic tone may ensure proper delivery of oxygen to embryonic tissues. Therefore, the peak in -blockade response on day 19 of
incubation may represent a heightened dependence on adrenergic systems
to protect against reduced oxygen supply, and this is simultaneous with
the increased capacity for catecholamine release (Table 5).
A surge in catecholamine levels at parturition is also part of the
mammalian ontogenetic repertoire that has been implicated to
participate in the process of absorption of lung fluid as well as
maintenance of glucose supply to the heart besides sustaining peripheral resistance (16). Thus it is conceivable that in
chickens catecholamines are involved in the timing of internal pipping by regulating the blood flow to the extraembryonic circulation and
ensuring adequate perfusion pressures to maintain gas exchange. As the
CAM begins to regress, before the onset of lung ventilation, the tonic
contribution of -adrenoreceptors may be important for maintaining
CAM perfusion. In addition, the established increase in catecholamine
concentration may be instrumental in the improvement of blood
oxygenation via an increase in synthesis of carbonic anhydrase and
2,3-diphosphoglycerate (7).
Perspectives
This study has delineated the basic mechanisms of cardiovascular control in embryonic chickens, which could be extended to the cardiovascular development of other vertebrate groups. Data from the present study indicate that vagal tone is absent throughout the ontogeny of chicken embryos. In addition, this work has established that the capacity for catecholamine release exhibits profound maturational changes during chicken ontogeny. This developmental change in catecholamine release ability is coupled to a constant-adrenergic tone on the heart and an -adrenergic tone on the vasculature that increases in magnitude as development progresses.
The absence of a clear vagal tone during embryonic development is not unique to the chicken. Fetal sheep have been shown in several studies to possess limited or no vagal tone during the latter third of gestation (24, 31, 32), possibly indicating that a lack of vagal tone is genetically dictated. An equally appealing alternative explanation is that the maturation of vagal tone is inversely related to the degree of maternal care, with embryos that are more exposed to environmental fluctuations showing a functional vagal tone on the heart earlier in development.
Even if vagal input is not critical to normal cardiovascular regulation
during development, the adrenergic system is clearly necessary. The
correlation between catecholamine concentrations and peak in
cardiovascular sensitivity further supports their importance in basal
cardiovascular function of embryonic chickens. Similar characteristics
are apparent in fetal sheep, which exhibit predominantly -adrenergic
activity with catecholamine levels peaking at term (2, 11,
24). Collectively, these data suggest that embryonic vertebrates
depend on hormonal adrenergic influence to control cardiovascular
activity and possibly to ensure successful embryonic life. Further work
is needed to delineate the degree to which these patterns are reflected
in other groups.
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ACKNOWLEDGEMENTS |
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We are greatly indebted to Gunilla Rydgren (Zoophysiology, University of Göteborg) for the HPLC analysis of catecholamine.
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FOOTNOTES |
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J. Altimiras was a recipient of a postdoctoral fellowship from the Danish Research Council. D. Crossley was supported by National Science Foundation Grant IBN-9616138 to W. W. Burggren and the Danish Center for Respiratory Adaptation.
Present address of J. Altimiras: Dept. of Zoophysiology, Univ. of Göteborg, Box 463, SE 405 30 Göteborg, Sweden.
Address for reprint requests and other correspondence: D. Crossley, Dept. of Ecology and Evolutionary Biology, Univ. of California at Irvine, Irvine, CA 92697 (E-mail: dcrossle{at}uci.com).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Received 27 December 1999; accepted in final form 8 May 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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A. H. Khandoker, K. Fukazawa, E. M. Dzialowski, W. W. Burggren, and H. Tazawa Maturation of the homeothermic response of heart rate to altered ambient temperature in developing chick hatchlings (Gallus gallus domesticus) Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2004; 286(1): R129 - R137. [Abstract] [Full Text]
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D. A. Crossley II, B. P. Bagatto, E. M. Dzialowski, and W. W. Burggren Maturation of cardiovascular control mechanisms in the embryonic emu (Dromiceius novaehollandiae) J. Exp. Biol., August 1, 2003; 206(15): 2703 - 2710. [Abstract] [Full Text] [PDF]
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D. A. Crossley II, W. W. Burggren, and J. Altimiras Cardiovascular regulation during hypoxia in embryos of the domestic chicken Gallus gallus Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2003; 284(1): R219 - R226. [Abstract] [Full Text] [PDF]
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K. Ruijtenbeek, J. G. R. De Mey, C. E. Blanco ;, and H. Ehmke The Chicken Embryo in Developmental Physiology of the Cardiovascular System: A Traditional Model with New Possibilities Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2002; 283(2): R549 - R551. [Full Text] [PDF]
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H. Scholz Adaptational responses to hypoxia Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2002; 282(6): R1541 - R1543. [Full Text] [PDF]
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M. C. Garofolo, F. J. Seidler, J. T. Auman, and T. A. Slotkin beta -Adrenergic modulation of muscarinic cholinergic receptor expression and function in developing heart Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2002; 282(5): R1356 - R1363. [Abstract] [Full Text] [PDF]
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A. L. M. Mulder, A. Miedema, J. G. R. De Mey, D. A. Giussani, and C. E. Blanco Sympathetic control of the cardiovascular response to acute hypoxemia in the chick embryo Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2002; 282(4): R1156 - R1163. [Abstract] [Full Text] [PDF]
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) and series
II (
) differed on day 20 of incubation, as indicated
by asterisk (P < 0.05). Data are plotted as mean
values ± SE.
) in MAP (A) and
fH (B) induced by a 5-min exposure to
10% O2 on each day of chicken incubation studied. An
asterisk indicates a significant response to hypoxia (P
value 0.0167). Like letters represent similar responses between days.
Data are plotted as mean absolute change ± SE; n = 6 embryos for each day.
