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1 Medical College, University of Nankai, Tianjin 300071, PR China 2 Division of Neuroscience, The Medical School, University of Birmingham, Birmingham B15 2TT, UK
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(Received 22 March 2006;
accepted after revision 10 May 2006; first published online 12 May 2006)
Corresponding author J. H. Coote: Division of Neuroscience, The Medical School, University of Birmimngham, Birmingham B15 2TT, UK. Email: j.h.coote{at}bham.ac.uk
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Introduction |
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Evidence suggests these PVN-spinal neurones are tonically active (Zhang et al. 1997; Zhang & Patel, 1998) and are synaptically influenced by stimulation of blood volume receptors (Lovick & Coote, 1988a,b, 1989). We recently showed that the PVN neurones influencing renal sympathetic nerve activity (RSNA) are subjected to a GABA-mediated inhibition, during atrial receptor stimulation to mimic volume load (Yang & Coote, 2003). The question arises, whether the PVN-spinal neurones contribute to an enhancement of RSNA induced by a reduction in blood volume produced by a venous haemorrhage (Clement et al. 1972). This has not been tested, however. Therefore, in the present study we examined the effects of pharmacologically blocking the spinal synapses of the PVN projection on an increase in RSNA produced by a mild venous haemorrhage in the rat.
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Methods |
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Animal preparation
The studies were conducted on 17 male Wistar rats weighing 313 ± 6.2 g. Animals were anaesthetized with a mixture of urethane and chloralose (650 and 50 mg kg–1, respectively) given I.V. after initial gaseous induction with enflurane O2 mixture. Anaesthesia was monitored by observing arterial blood pressure (BP) and heart rate (HR) and by the absence of corneal and paw-pinch reflexes, and an adequate depth was maintained by regular administration of additional anaesthetic (I.V.) as required.
A femoral artery was cannulated with a polyethylene catheter (PE-50 tubing), which was connected to a pressure transducer for continuous recording of arterial blood pressure. A femoral vein was cannulated for administration of drugs. Electrocardiogram (ECG) signals were obtained from an ECG monitor via two platinum wire electrodes inserted under the skin of the limbs. The trachea was cannulated and spontaneous respiration maintained throughout the experiment. Rectal temperature was continuously monitored and maintained at 37°C by a heating blanket.
Spinal cord perfusion
The spinal subarachnoid space was cannulated for the intrathecal (I.T.) administration of drugs. After the rat was placed in a stereotaxic frame (Narishige), the atlanto-occipital membrane was exposed by removing the overlying muscle through a dorsal mid-line incision. A laminectory was performed at C1 to provide clear access for the intrathecal catheter. A 14 cm length of PP-10 tubing (total volume, 15 µl) filled with artificial cerebrospinal fluid (ACSF; containing (g): NaCl, 7.42; KCl, 0.14; KH2PO4, 0.163; CaCl2, 0.22; MgSO4, 0.319; NaHCO3, 2.18; and glucose, 1.8; in 1 l distilled water; pH 7.4) was introduced under the dura mater and advanced 5.5 cm caudally along the dorsal surface so that the tip lay over the T10 segment. The position was confirmed at the end of the experiment. Drugs were administered in a volume of 10 µl and washed in with 20 µl of ACSF. Each infusion took up to 1 min. The following drugs were used: L-glutamic acid (Sigma); kynurenic acid (4-hydroxyquinoline-2-carboxylic acid (Sigma); (Arg8)-vasopressin (AVP, Sigma); V1a antagonist ([ß-mercapto-ß,ß-cyclopentamethylene proprionyl1,-O-Et-Tyr2,Val4,Arg8]-vasopressin; Sigma). Throughout the Results, the amount of drug is given by the volume and molar concentration of each injection. All solutions were made immediately prior to use and pH was adjusted to 7.4.
Recording sympathetic nerve activity
The left kidney was exposed retroperitoneally and, with the aid of an operating microscope, a branch of the sympathetic nerve to the kidney was dissected free and placed on a bipolar silver-wire electrode. After the condition for optimal nerve recording had been established, both the nerve and the electrode were covered in paraffin. The neural signals were amplified (gain, 5000; Neurolog, Digitimer, Welwyn Garden City, Herts, UK), filtered (50 Hz low frequency, 3000 Hz high frequency; Neurolog) and displayed on an oscilloscope, and collected for displaying and later analysis using a PowerLab data acquisition system (AD Instruments).
Experimental protocol
After recording stable baseline levels of BP, HR and RSNA for 15 min, the effect on RSNA of I.T. application of ACSF (10 µl), and of vasopressin or glutamate agonists and antagonists were tested in sequence, with 15 min recovery between each test. A mild haemorrhage was next produced by withdrawing 1 ml of blood into a heparinized syringe, over 1 min from a femoral vein. The blood was reinfused 5 min later. After a further 15 min (providing BP and RSNA were not significantly different from control baseline), a second haemorrhage test was performed. After these initial procedures, the effect of I.T. ACSF or I.T. pharmacological antagonists on the RSNA response to haemorrhage was tested. Agents were given I.T. 1 min prior to withdrawing 1 ml of blood from the femoral vein. Following reinfusion of blood, a 15 min recovery period, or longer until BP and RSNA were not significantly different from control values, was allowed to elapse before further tests. In every animal, the effect of an antagonist given intrathecally was tested at least three times (unless otherwise stated), either alone or following haemorrhage. At the end of experiments rats were killed by an overdose of anaesthetic (urethane/chloralose).
Data analysis
Using a PowerLab8SP AD Instruments processor and Chart v4.0 software, BP, RSNA and ECG were recorded on-line. All data were digitized at 1 kHz and stored in a Power Macintosh G4 personal computer (Apple) for on-line or off-line processing. Responses of RSNA were expressed as a percentage change compared to the basal value immediately before each test. For this purpose, the raw nerve signal was passed through a spike discriminator (PowerLab) to remove background noise and then the total nerve activity, in spike counts per second, from the time that it changed from the basal value to the time when it reached a maximum value, was computed and compared to the value during a similar period before each test. Only experiments in which the level of background noise was confirmed at the end of the experiment following terminal anaesthesia are included in this report. All data are expressed as means ± S.E.M. Statistical analysis was performed using a Mann–Whitney U test, after first subjecting the data to a two-way repeated measure ANOVA. Statistical significance was considered to be reached at P < 0.05.
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Results |
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In four of this series of 17 rats, prior to haemorrhage tests, the action of glutamate and vasopressin and their antagonists, which we have previously documented, was confirmed (Fig. 1A; Yang et al. 2002). Intrathecal application of AVP (10 µl, 0.01 mM) increased RSNA by 28 ± 4%, and this was significantly reduced to 2 ± 2% (P < 0.01) by prior I.T. application of the V1a antagonist (10 µl, 0.05 mM). Similarly, I.T. glutamate (10 µl, 200 mM) increased RSNA by 31 ± 4%, and this was abolished by prior application of kynurenic acid (10 µl, 4 mM; P < 0.01). Kynurenic acid (I.T.) had no significant effect on the excitation of RSNA produced by AVP, nor did the I.T. application of the V1a antagonist significantly change the effect of I.T. glutamate.
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In 17 rats (mean BP, 82 ± 2 mmHg), removal of 1 ml of venous blood caused a fall in BP of 7 ± 0.7 mmHg accompanied by an increase in RSNA of 26 ± 2%, a change that was significantly above control baseline activity (P < 0.01; Figs 1B and 2A). Five minutes after reinfusion of blood, RSNA recovered to 3.4 ± 2.3% above the control baseline level, from which it was not significantly different. At the same time, BP had not fully recovered, being 6 ± 0.5 mmHg below control values. By 15 mins after reinfusion of blood, however, the mean BP was within 1 ± 0.5 mmHg of the prehaemorrhage value.
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Following intrathecal application of the V1a antagonist (10 µl, 0.05 mM), a haemorrhage which reduced BP by 6.7 ± 1 mmHg had significantly less effect on RSNA, this being 13 ± 4% increased, a reduction of 50% compared to haemorrhage alone (P < 0.01, Fig. 2B). Similar intrathecal application of the V1a antagonist or ACSF, tested alone without haemorrhage, had no significant effect on RSNA or BP. Five minutes after reinfusion of blood, RSNA was 6 ± 4% (P < 0.05) below the control baseline level but by 15 mins was not significantly different. Arterial blood pressure had also recovered during this period.
Glutamate involvement
Two doses of the broad spectrum glutamate antagonist kynurenic acid were tested, 4 mM in 17 rats and 2 mM in eight of these rats.
Intrathecal application of 4 mM kynurenic acid (10 µl) caused a small reduction in baseline RSNA of 6 ± 1% (P < 0.05 compared to control values). Therefore, the postkynurenic acid baseline was used when estimating the effect of the antagonist on an increase in RSNA induced by haemorrhage. The changes were then compared to those induced prior to kynurenic acid. In 17 rats, application of 4 mM kynurenic (10 µl, I.T.), prior to haemorrhage which reduced BP by a mean of 7 ± 1.7 mmHg, resulted in a significant attenuation of the RSNA response, which now increased only by 13 ± 3% from the level of RSNA postkynurenic acid (Fig. 2C). This was less than half the increase of 28 ± 2% in RSNA induced by haemorrhage prior to kynurenic acid (P < 0.01). Five minutes after reinfusion of blood, RSNA was not significantly different from control values, whereas BP did not return to the control level until 15 min. A 10 µl intrathecal application of 2 mM kynurenic acid given alone had no significant effect on baseline RSNA in eight of the 17 rats in which its action was tested. Following this dose of kynurenic acid, the RSNA increase in response to haemorrhage was 25 ± 5.5%, which was not significantly different from the increase in RSNA in response to haemorrhage alone.
Vasopressin and glutamate
In 11 of the 17 rats, after a series of tests with each of the antagonists, the combined effect of the V1a antagonist (0.05 mM, 10 µl I.T.) immediately followed by kynurenic acid (4 mM, 10 µl I.T.) was tested (one or more times if the experimental conditions allowed). This combination caused a small reduction in RSNA but this was not significantly different from that induced by kynurenic acid alone. Haemorrhage alone increased RSNA by 27 ± 2%. However, application of the two antagonists prior to haemorrhage caused a significant reduction of the RSNA response to haemorrhage (which reduced BP by 6.5 ± 1 mmHg), to 8 ± 3%. This was significantly different compared to haemorrhage alone (P < 0.01) and compared to haemorrhage plus V1a alone and haemorrhage plus kynurenic acid alone (P < 0.05) but not significantly different from the control baseline level (Fig. 2D). Both BP and RSNA had not recovered by 15 min after reinfusing blood, but in six rats by 30 min both were not significantly different from control levels and a further test was completed. In the other five rats, recovery was not achieved and the experiments were terminated.
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Discussion |
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The study showed that the increase in RSNA was significantly reduced by application of a highly selective V1a antagonist (Yang et al. 2002) to the thoracic spinal cord. Therefore, we conclude that part of the reflex increase in RSNA in response to blood volume reduction was mediated by spinal vasopressin receptors. This is strongly supported by the demonstration that the V1a antagonist given intrathecally at the same dose effectively blocked an excitatory action of intrathecal vasopressin but was without effect on a similar excitatory action of intrathecal glutamate, which confirms the findings of our previous study (Yang et al. 2002). The origin of supraspinal vasopressin neurones is most likely to be the PVN, since there is much evidence that this nucleus is a major source of these parvocellular neurones (Buijs, 1978; Sawchenko & Swanson, 1982; Lang et al. 1983; Cechetto & Saper, 1988; Hallbeck & Blomqvist, 1999; Huang & Weiss, 1999; Motawei et al. 1999). Also, we have previously shown that a PVN-induced increase in RSNA is selectively blocked by the intrathecal application of the same V1a antagonist used here (Yang et al. 2002). Furthermore, parvocellular neurones in the PVN are activated by haemorrhage (Krukoff et al. 1997) and hypovolaemia (Badoer et al. 1993). However, according to a study of the central nervous effects of hypovolaemia in conscious rabbits (Potts et al. 2000), activated neurones in the PVN, immunolabelled for Fos, were not immunoreactive for vasopressin, whereas neurones in the supraoptic nucleus (SON) were double labelled. Therefore, it was concluded that PVN vasopressin neurones did not participate in the response to a reduction in blood volume. Since there is no evidence that SON neurones project to the spinal cord (Holstege, 1987; Strack et al. 1989; Schramm et al. 1993; Huang & Weiss, 1999), the present results are at variance with this view. The explanation may lie in a possible failure by Potts et al. (2000) to label vasopressin in the smaller parvocellular spinally projecting neurones in the PVN. Unfortunately, the study by Potts et al. (2000) does not comment on the type of labelled cells in the PVN. This is important because parvocellular vasopressin neurones appear to be less easy to identify immunologically than magnocellular neurones, a feature which may have contributed to the wide variations in estimates of this spinal projection by several groups (Sawchenko & Swanson, 1982; Cechetto & Saper, 1988; Hallbeck & Blomqvist, 1999; Huang & Weiss, 1999).
The evidence of the present study also showed that a supraspinal vasopressin pathway is not alone in mediating the reflex response to haemorrhage, since the increase in RSNA was also partly attenuated by intrathecal application of the broad spectrum ionotropic glutamate receptor antagonist kynurenic acid. It is unlikely that this can be attributed to a non-selective action of kynurenic acid because it was shown that similar doses of the antagonist are ineffective in preventing the excitatory action of vasopressin, confirming our recent study (Yang et al. 2002). Therefore it seems likely that glutamate neurones are in some way involved. This could be a consequence of a strong dependence of spinal vasomotor neurones on tonic glutamate excitatory drive from rostral ventrolateral medullary (RVLM)-spinal neurones (Morrison et al. 1991; Deuchars et al. 1995). Thus, we observed that after kynurenic acid, RSNA baseline level was slightly reduced. However, this appears insufficient to account for the magnitude of attenuation of the haemorrhage response induced by kynurenic acid, which was more than half of the control response. This could indicate that the reflex RSNA increase also depends on direct activation of a glutamate releasing pathway, either via the PVN or more directly via medullary pathways to RVLM. Consistent with this are studies showing that haemorrhage activates RVLM-spinal neurones (McAllen et al. 1992; Dun et al. 1993), although the blood loss in these studies was more severe than that of the present study.
As well as these considerations, suggesting that two chemically distinct populations of supraspinal neurones converge onto the renal sympathetic outflow, there is also the possibility that glutamate is coreleased with vasopressin at the spinal synapses of the PVN-spinal neurones. It is intriguing that in our other studies, we found that activation of renal nerve sympatho-excitatory sites in the PVN were partly antagonized at the spinal level by either V1a antagonist or by the glutamate antagonist kynurenic acid (Yang et al. 2002). Similarly, in a previous study, we showed that PVN-induced excitation of identified single RVLM-spinal vasomotor neurones was selectively antagonized by either of these agents (Yang et al. 2001). Although this dual effect of PVN activation could also be caused by stimulation of two neuronal phenotypes, by a large volume of excitatory amino acid D,L-Homocysteic acid (DLH) in the latter studies (Yang et al., 2001, 2002), it would appear from the present results that a more physiological stimulus, like hypovolaemia, does the same. In the absence of more substantial evidence, however, these considerations must remain speculative.
A further feature of this study concerns the peripheral sensory receptors involved in detecting the withdrawal of 1 ml of venous blood. Based on a mean blood volume of 64 ml kg–1 in the rat (Anselmo-Franci et al. 1998), 1 ml represented about 5% of total blood volume. This is a small amount compared to most previous studies on the role of the brain in the physiological changes during haemorrhage, in which 10% or more of total blood volume was removed (e.g. Gomez et al. 1993; Krukoff et al. 1995; Anselmo-Franci et al. 1998). Also, in many studies, this has been achieved by removing arterial blood (e.g. Togashi et al. 1990; McAllen et al. 1992; Badoer et al. 1993; Dun et al. 1993). Many of the studies were designed to elicit falls in blood pressure. In the present study, we wished to minimize falls in blood pressure and as far as possible to restrict the stimulus to the low-pressure receptors at the vein–atrial junctions. These receptors are likely to be capable of detecting a 5% change in venous return, since over their response range they display a threefold increase above threshold for a unit change in stretch and are active at normal atrial pressures (Thoren et al. 1979; Mifflin & Kunze, 1982). Therefore, we presumed that removal of venous blood would primarily effect the atrial receptors, which undoubtedly have actions on PVN neurones (Badoer et al. 1993; Potts et al. 2000; Pyner et al. 2002; Yang & Coote, 2003). However, whether the reflex increase in RSNA was entirely due to a reduction of the atrial receptor input may be questioned, since the hypovolaemia did result in small falls in blood pressure and these would have reduced arterial baroreceptor input. It seems, though, that the latter receptors are of less significance in the response to mild haemorrhage, since their removal has no effect on the number of neurones activated in the hypothalamus and medulla (Potts et al. 2000).
In conclusion, we consider that the study shows that hypovolaemia results in reflex activation of supraspinal vasopressinergic and glutaminergic neurones that increase the activity in renal sympathetic nerves. These data support the hypothesis that PVN-spinal vasopressin presympathetic neurones are a key component of a plasma volume control system.
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References |
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