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Departments of 1 Physiology and 2 Otorhinolaryngology, Mie University School of Medicine, Tsu, Mie 514-8507, Japan
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In stressful conditions, baroreflex vagal bradycardia (BVB) is often suppressed while blood pressure is increased. To address the role of the rostral ventrolateral medulla (RVL), a principal source of sympathetic tone, in inhibition of BVB, we microinjected DL-homocysteic acid (DLH, 6 nmol) into the RVL of chloralose-urethan-anesthetized, sinoaortic-denervated rats to examine the effect on BVB. The BVB was provoked by electrical stimulation of the aortic depressor nerve ipsilateral to the injection sites. DLH microinjection was found to suppress BVB while increasing blood pressure. The inhibition of BVB was observed even during the early phase in which DLH transiently suppressed central inspiratory activity. The inhibition was not affected either by upper spinal cord transection or suprapontine decerebration. Similar results were obtained by microinjection of bicuculline methiodide (160 pmol), a GABA antagonist, into the RVL of carotid sinus nerve-preserved rats due to withdrawal of a tonic GABA-mediated, inhibitory influence including the input from arterial baroreceptors. In conclusion, activation of the RVL inhibits BVB at brain stem level independently of central inspiratory drive.
aortic depressor nerve; DL-homocysteic acid; 
-aminobutyric acid; bicuculline; sympathetic-parasympathetic
interaction
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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ARTERIAL BAROREFLEXES, especially the vagal heart rate component, are known to be suppressed in stressful conditions (see Ref. 22 for review). For examples, baroreflex vagal bradycardia (BVB) is reflexly inhibited by somatic (24) as well as visceral nociceptive inputs (23). Similar effect is produced by activation of some central nervous structures, such as hypothalamic defense area (2) or dorsolateral part of the periaqueductal gray matter (PAG) (9, 25). Since inhibition of BVB induced by these perturbations always accompanies an increase in blood pressure, it is a natural question whether activation of the rostral ventrolateral medulla (RVL), a pivotal source of sympathetic vasomotor tone (4), has an inhibitory influence on BVB as well. This question may involve potential occurrence of sympathetic vagal interaction at brain stem level.
There have been a few reports regarding the RVL influence on BVB. Zhang et al. (37) described that microinjection of glutamate into the RVL region produced pressor and bradycardiac responses; it augmented sensitivity of BVB induced by intravenous phenylephrine. According to Lin et al. (18), however, microinjection of angiotensin II into the RVL, which is known to excite presympathetic neurons there (17) by decreasing potassium conductance (16), thereby increasing blood pressure (18), suppressed baroreflex bradycardia induced by intravenous phenylephrine. The suppression was reversed to facilitation following administration of angiotensin receptor antagonists (18). Collectively, the role of the RVL in modification of BVB remains unsettled.
The present study was designed to address the important but yet
controversial issue of whether the RVL, a region that contains presympathetic neurons, affects BVB or, in a broader sense, the vagal
cardioinhibitory mechanism at the medullary level. Using totally
baroreceptor-denervated Wistar rats, we chemically stimulated the RVL
by microinjection of DL-homocysteic acid (DLH), a
broad-spectrum excitatory amino acid agonist. Under 
-adrenergic
receptor blockade, the aortic depressor nerve (ADN) was stimulated to
produce BVB, and the effect of RVL activation on the BVB was studied.
With this method, the test baroreceptor input could be held constant no
matter how much blood pressure was changed during the conditioning challenge. The result was supplemented by another series of
experiments, in which bicuculline methiodide, a GABA A receptor
antagonist, was microinjected into the RVL of rats with the carotid
sinus nerve uncut, and the effect was examined on BVB. Bicuculline
microinjection into the RVL was expected to activate the presympathetic
neurons, thereby removing the tonic GABA-mediated inhibition, including the baroreceptor-dependent one (4).
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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General procedures.
Experiments were performed in male Wistar rats, weighing 350-400
g, anesthetized with intraperitoneal injection of 
-chloralose (60 mg/kg) and urethan (600 mg/kg). Polyethylene tubes were introduced into
the left femoral artery and vein for blood pressure monitoring and drug
administration, respectively. One-sixth of the initial dose was
intravenously supplemented every 3 h. The adequacy of this
anesthetic recipe had been ascertained by the lack of an avoidance
reaction to hind paw pinching under conditions of spontaneous breathing. Animals were immobilized with intravenous succinylcholine (initially 10 mg/kg, supplemented with one-half the dose as needed) and
artificially ventilated with room air through a tracheal cannula. After
the immobilization, adequate anesthetic conditions were assured
according to the stability of blood pressure and heart rate. Throughout
the experiment, -adrenergic receptors were blocked with intravenous
injection of propranolol (initially 0.5 mg/kg, supplemented with
one-half the initial dose on appreciable increase in resting heart
rate). With this blockade, a heart rate change could be attributed to a
change in the vagal activity to the heart.
DLH microinjection study. In this series of experiments, the carotid sinus nerve beside the ADN was sectioned bilaterally. Chemical stimulation of the neurons in the RVL was made by pressure microinjection of DLH through a glass capillary micropipette (tip diameter, 20 µm) on the side ipsilateral to ADN stimulation. DLH was dissolved in 4:1 admixture of Ringer solution and 0.2 M phosphate buffer solution (pH 7.4) at a concentration of 30 mg/ml (160 mM). For marking the injection sites, ferritin (10% solution) was added in the solution (20 ~ 30 µl/ml). The final pH was adjusted to 7.4 with 0.1 N NaOH. Each injection delivered 6 nmol DLH in 40 nl. Stereotaxic coordinates of the RVL for injection were 2,500-3,000 µm rostral to the calamus scriptorius, 2,500-3,000 µm ventral to the surface, and 2,000-2,500 µm lateral to the midline. After a blood pressure response to DLH microinjection reached the plateau level, test ADN stimulation was applied to examine the DLH effect on BVB. In some animals, the spinal cord was subsequently cut at the C2 level to evaluate the possible prejunctional inhibitory influence through the cardiac sympathetic nerve on acetylcholine release from the cardiac vagus terminals (15). The resultant hypotension was compensated for by intravenous infusion of Ringer solution containing 3% dextran to maintain the blood pressure level above 60 mmHg. Furthermore, suprapontine decerebration was made by transecting the exposed brainstem rostral to the parabrachial region using a fine spatula under a dissecting microscope to examine the contribution of the forebrain structures to RVL influence on BVB. The ineffectiveness of microinjection of the vehicle solution containing ferritin but devoid of DLH was confirmed in advance.
The structures in the rostral medulla other than the RVL were also tested with DLH microinjection to examine their effect on BVB.Bicuculline microinjection study. The RVL is under tonic, GABA-mediated inhibition by baroreceptor-dependent input (4). Thus additional experiments were performed to activate the RVL neurons by removing the GABA inhibition. In this experiment, the carotid sinus nerve was left uncut to preserve the ongoing, baroreceptor-originated input to the caudal ventrolateral medulla (CVL). To remove GABA inhibition, bicuculline methiodide, a GABA antagonist, was microinjected into the RVL ipsilateral to ADN stimulation. Preparation of the solution for microinjection was the same as for DLH. Bicuculline methiodide was dissolved in the 4:1 admixture of Ringer solution and phosphate buffer (pH 7.4), at a concentration of 1 mg/ml (2 mM). For marking the injection sites, ferritin was added as well. The pH was not necessary to adjust. Injection volume was 80 nl containing 160 pmol of bicuculline methiodide. In some rats, the spinal cord was then cut at C2 level, and the bicuculline effect on BVB was compared before and after the section.
Injection sites. At the end of each experiment, animals were killed with exsanguination by bilaterally cutting the common carotid arteries; the brain was removed and fixed in 7% Formalin. Sections of 70 µm in thickness were prepared on a freezing microtome, and ferritin iron that had been deposited in the brain tissue was histochemically visualized according to the Prussian blue method. All the sections were counterstained according to the method of Tolivia and Tolivia (35). Locations of the injection sites were plotted on a histology-based stereotaxic atlas (29).
Data analysis. Magnitude of BVB was expressed as the decrement of heartbeats due to electrical stimulation of the ADN. Inhibition or facilitation of BVB by a conditioning stimulation was shown as a percentage of ratio of the resultant change in the heartbeat decrement of the test BVB to that of control BVB (24).
All the numerical data obtained in the experiments were given as means ± SE. Data from multiple groups were first analyzed according to the Kruskal-Wallis test. Intergroup differences were then analyzed by the Wilcoxon signed rank or Mann-Whitney U test, depending on paired or unpaired comparison, respectively; differences were regarded as significant when P was <0.05.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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DLH stimulation of the RVL.
After DLH microinjection to the RVL region, blood pressure elevated
promptly, reached the peak level within 20-40 s, and gradually declined to the original level (Fig. 1).
Magnitude of the blood pressure increase was 50 ± 2 mmHg (initial
level, 81 ± 4 mmHg; peak values, 131 ± 4 mmHg, n = 13).
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Changes in central inspiratory drive.
To address whether a change in central inspiratory drive was involved
in the inhibition of BVB, the phrenic nerve discharges were recorded in
four rats on the side contralateral to the RVL injected with DLH. We
found that phrenic nerve discharges were suppressed immediately on DLH
injection. The suppression lasted 20-40 s, gradually turning to
facilitation. Even during the inspiratory suppression, inhibition of
BVB was still observed (Fig.
3A). After bilateral vagotomy,
it was evident that DLH given to the RVL inhibited central inspiratory
drive (Fig. 3B).
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DLH stimulation of sites other than the RVL.
Besides the RVL, we microinjected DLH to other sites in the rostral
medulla at the level of 2,500 µm rostral to the calamus scriptorius.
A number of the nuclei produced inhibition of BVB as well as blood
pressure increase. The sites included the following: the lateral
paragigantocellular reticular nucleus, the gigantocellular reticular
nucleus, the raphe nuclei obscurus/pallidus, the lateral tegmental
reticular formation (parvocellular reticular nucleus plus intermediate
reticular nucleus), and the spinal trigeminal nucleus. The results are
collectively provided in Table 1. The injection sites with their responsiveness are shown in Fig.
4.
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Bicuculline disinhibition of the RVL.
If the DLH inhibition of BVB involves presympathetic neurons in the
RVL, then application of a GABA antagonist, which removes baroreceptor-dependent, GABA-mediated inhibition of these neurons (4), should inhibit BVB as well. To address this issue, we used the rats with the carotid sinus nerve intentionally preserved. As
shown in Fig. 5, bicuculline
microinjection to the RVL gradually increased blood pressure from basal
level of 94 ± 4 mmHg to peak level of 132 ± 4 mmHg
(n = 27), with net increase being 37 ± 2 mmHg.
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Responses of other sites to bicuculline injection.
In addition to the RVL, the raphe nuclei were another structure in the
rostral medulla that produced inhibition of BVB on bicuculline
microinjection. After bicuculline injection, the raphe nuclei showed
slight to moderate hypertension (13 ± 4 mmHg, n = 10) and inhibition of BVB of variable degrees (percentage of inhibition, 37 ± 10%; Fig. 8).
Unlike the RVL, however, bicuculline injection into the nuclei did not
appear to affect baroreflex hypotension.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In the present study, BVB was induced by electrical stimulation of
the ADN under -adrenergic receptor blockade, and the magnitude of
the bradycardia was taken as not only the index of heart rate component
of baroreflexes but also the index of cardiovagal outflow. According to
our experience, BVB thus induced in rats is pronounced, sometimes
leading to cardiac arrest. We admit that the best approach of
evaluating a given effect on cardiovagal outflow would be determination of the effect on unitary responses or field potentials antidromically activated by stimulation of identified cardiac branches of the vagus.
In practice, however, this is subject to technical limitation, since
the cardiovagal preganglionic neurons in rats are dispersed without
forming a distinct nuclear organization (26). Instead, the
BVB produced by ADN stimulation is considered to provide a currently
most convenient, reproducible measure of cardiovagal activity.
The present study has shown that the RVL, when activated either directly by excitatory amino acid or through disinhibition by a GABA antagonist, inhibits BVB. The implications of this finding are twofold, one regarding central modification of BVB and the other regarding sympathetic-vagal interaction. In terms of the former issue, there have been a number of reports delineating sites in the central nervous system that suppress or facilitate BVB (see Ref. 22 for review). The sites inhibiting BVB include the following: the cerebral motor cortex (1), the hypothalamus (2), the amygdala (32), dorsolateral part of the PAG (9, 25), the parabrachial nucleus (14, 21, 30), and cerebellar posterior vermis (13, 28). The sites facilitating BVB include the following: the medial prefrontal and insular cortices (27, 31, 36), the preoptic area (8), lateral hypothalamic area (8, 27), ventrolateral part of the PAG (7), and the nucleus raphe magnus (7). In addition to these sites, the present study showed that a number of brain stem structures, especially the RVL, are involved in inhibition of BVB. This accords with a recent observation that the RVL mediates the inhibition of BVB provoked by a more rostral portion of the brain (14).
As the second implication, the finding that excitation of the RVL is accompanied by reduction of vagal outflow is considered to suggest the presence of sympathetic-vagal interaction within the brain stem. Although the mechanism is so far unknown, circadian or occasional reversal of reciprocal tones of sympathetic and parasympathetic divisions is a fundamental property of the autonomic nervous system. Our observation that the RVL inhibits vagal activity within the brain stem seems to offer an important clue for understanding the mechanism underlying the creation of an ergotropic phase in which sympathetic activity dominates over vagus activity. This view is at present a hypothetical one, because the RVL is not a homogenous structure but contains neurons other than presympathetic neurons. Above all, the presence of respiratory neurons in the RVL calls for special caution since the central inspiratory drive is known to suppress BVB (5). In the present study, however, DLH microinjection in the RVL immediately suppressed inspiratory activity as measured by phrenic nerve activity. During the phase of inspiratory suppression, BVB was still inhibited. The inspiratory suppression was likely due to activation of those expiratory neurons in the Bötzinger complex, which are known to suppress the activities of overall inspiratory neurons (3). The location of Bötzinger expiratory neurons overlaps that of presympathetic neurons in the RVL (11). Occurrence of inhibition of BVB even during this inspiratory suppression implies that the inhibition does not necessarily depend on the facilitated inspiratory drive.
Another important problem is that the inhibition of BVB could only be produced by those neurons that are inhibitory in nature. They could be those inhibitory, expiratory neurons in the Bötzinger complex as mentioned above. However, this view apparently contradicts with the fact that BVB is inhibited in inspiratory phase, not in expiratory phase (5), although their possible involvement in DLH or bicuculline inhibition of BVB is not entirely ruled out. Alternatively, presympathetic neurons in the RVL could indirectly inhibit vagal cardioinhibitory neurons provided that inhibitory neurons intervene between them. Such excitatory-inhibitory conversion may be achieved by GABAergic neurons extensively populated in the medullary reticular formation (10).
Morphological background for the possible intramedullary interaction of the RVL neurons on the vagal activity has been provided by a recent electrophysiology-based anatomical study. Lipski et al. (19) identified "barosensitive" neurons in the RVL that generated inhibitory postsynaptic potentials on electrical stimulation of the ADN and intracellularly labeled them with a tracer dye to examine their morphology. The labeled RVL neurons issued axons that directed dorsomedially and then rostrally or caudally, or coursed directly caudally. Some of them issued thin and short axon collaterals in their medullary course, in the areas dorsal to the RVL, in the dorsal vagal complex, or in the CVL. Projection of these axon collaterals to certain inhibitory neurons might be responsible for the inhibition of BVB by the RVL as revealed in the present study.
The findings of our present study contradict those reported by Zhang et al. (37). These authors microinjected glutamate into the RVL in Sprague-Dawley rats and found that resultant profound hypertension was accompanied by a brisk vagal bradycardia. This bradycardia was considered to be baroreceptor-mediated because it was eliminated by sinoaortic denervation, but the magnitude was greater than baroreflex bradycardia evoked by comparable hypertension induced by intravenous phenylephrine. Also, phenylephrine-induced bradycardia was potentiated by glutamate microinjection into the RVL. The controversy between their studies and ours may be partly but not satisfactorily be explained by differences in rat strains (Sprague-Dawley vs. Wistar), in anesthesia (chloralose vs. chloralose-urethan), in conditions of baroreceptor afferent nerves (preserved vs. transected), or in excitatory amino acids injected (glutamate vs. DLH). Instead, a plausible explanation may be made based on differences of injection sites in rostrocaudal direction. We injected DLH along the track at the level 2,500-3,000 µm rostral to the calamus scriptorius, whereas Zhang et al. (37) injected glutamate at the level 2,000 µm rostral to the calamus. Considering that the vagal cardioinhibitory neurons in rats are distributed at levels from 500 to 1,500 µm rostral to the calamus (26), glutamate injected in the coordinates of Zhang et al. (37) could reach by diffusion the rostral population of cardiovagal preganglionic neurons in addition to activating the RVL neurons. Elimination of the hypertension-associated bradycardia following sinoaortic denervation is accounted for by withdrawal of converging effects of excitatory baroreceptor influence and direct glutamate action on the cardiovagal preganglionic neurons. Sensitization of phenylephrine-induced BVB by glutamate injection is likewise explained in terms of convergence.
Later, it was reported from the same laboratory that a glutamate uptake inhibitor, which increases extracellular concentration of endogenously released glutamate, enhances phenylephrine-induced BVB (20). This effect, however, cannot be attributed to activation of the presympathetic neurons in the RVL, since basal blood pressure was not increased by this procedure. This was probably because the RVL neurons do not receive appreciable amount of tonic glutamatergic input in anesthetized condition (4). In contrast, cardiovagal preganglionic neurons are proposed to receive tonic glutamatergic input derived from ongoing baroreceptor activity (6). Therefore, the enhancement of BVB by the glutamate uptake inhibitor is likely caused by its diffusion to, and action on, the vagal preganglionic neurons or, alternatively, by activation of a nearby yet unknown baroreflex-sensitizing mechanism.
In the present study, we found that a pressor response and inhibition of BVB were produced not only from the RVL but also from a variety of regions on DLH microinjection. There was a tendency for the ventral-to-lateral portion to provoke these responses relatively more frequently and markedly. Suppose that the RVL is the site of prime importance for these responses, then the rather diffuse distribution of the responsive sites is partly explained by the widespread expansion of dendrites of the RVL neurons as morphological studies have shown (19, 33, 34). Alternatively, the pressor response and inhibition of BVB obtained from part of the reticular formation may be related to those as observed following nociceptive stimulation. The medullary reticular formation is the site of integration of a variety of ascending and descending information; especially, the somatic nociceptive input, which ascends along complex pathways (24), may in part terminate there to cause a variety of autonomic responses on the way to the forebrain. Inhibition of BVB produced by DLH stimulation of the spinal tract nucleus of the trigeminal nerve is possibly related to the inhibition responding to noxious input along the trigeminal nerve (12).
Inhibition of BVB produced by bicuculline microinjection deserves a special mention. The bicuculline-induced GABA A receptor blockade in the RVL increased blood pressure and inhibited BVB. These responses could be attributed to disinhibition of the RVL neurons, including removal of baroreceptor-dependent inhibitory input (4). This notion was supported by the finding that following bicuculline, baroreflex hypotension became progressively attenuated as blood pressure elevated with time, whereas the inhibition of BVB became augmented. In contrast, inhibition of BVB produced by microinjection of bicuculline into the raphe nuclei was apparently unrelated to sympathoexcitation due to impairment of baroreflex circuitry, because it was not accompanied by attenuation of baroreflex hypotension. It is suggested that the raphe neurons have a potential inhibitory action on the cardiovagal outflow system, but this action may be tonically masked because of a certain GABA-mediated inhibition.
In conclusion, the RVL inhibits BVB when activated directly by excitatory amino acid or through removal of GABA-mediated inhibitory input, including the baroreceptor-dependent one. The inhibition does not necessarily depend on central inspiratory drive. Future studies are needed to identify the neurons of the RVL responsible for the inhibition and to determine the exact nature of the interaction between the RVL and cardiovagal mechanism.
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ACKNOWLEDGEMENTS |
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This study was supported by a Grant-in-Aid for Scientific Research (C) from the Ministry of Education, Science, Sports, and Culture, Japan.
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FOOTNOTES |
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Address for reprint requests and correspondence: S. Nosaka, Mie Univ. School of Medicine, Dept. of Physiology, Edobashi 2-174, Tsu, Mie 514-8507, Japan (E-mail: snosaka{at}doc.medic.mie-u.ac.jp).
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. Section 1734 solely to indicate this fact.
Received 11 May 1999; accepted in final form 8 March 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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