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Department of Environmental Health, Life Science and Human Technology, Nara Women's University, Kita-Uoya Nishimachi, Nara, 630-8506, Japan
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Abstract |
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(Received 21 September 2003;
accepted after revision 11 March 2004;
first published online 12 March 2004)
Corresponding author K. Miki: Life Science and Human Technology, Nara Women's University, Kitauoya-Nishimachi, Nara 630-8506, Japan. Email: k.miki{at}cc.nara-wu.ac.jp
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Introduction |
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Futuro-Neto & Coote (1982) demonstrated that there were reductions in the activities of the greater splanchnic, inferior cardiac, lumbar sympathetic and renal sympathetic nerves, while there was an increase in activity in sympathetic fibres to the gastrocnemius muscle during REM sleep-like periods induced by physostigmine sulphate in mid-collicular decerebrate cats. This suggested the possibility that diverse changes in sympathetic nerve activity (Simon & Riedel, 1975) might occur during REM sleep and the increase in systemic arterial pressure could be caused by increased resistance of the muscle vascular bed, which might be sufficient to overcome the decreased vascular resistance of the visceral organs. Indeed, in humans, an increase in muscle sympathetic nerve activity, measured using microneurography, has been reported during REM sleep (Okada et al. 1991; Somers et al. 1993). However, it is impossible to measure visceral sympathetic nerve activity during REM sleep in man at present, which limits evaluation of potential divergent patterning of sympathetic outflow during REM sleep. In animal studies, since the report by Futuro-Neto & Coote (1982), to our knowledge, no reports have been made of the measurement of muscle sympathetic nerve activity during REM sleep. Therefore, direct measurement of muscle sympathetic nerve activity during REM sleep in normally behaving animals would provide key evidence for the mechanisms underlying the increase in systemic arterial pressure during REM sleep.
The purpose of the present study was to measure muscle sympathetic nerve activity and muscle blood flow during REM sleep in nonanaesthetized chronically instrumented rats. To achieve this aim, lumbar sympathetic nerve activity (LSNA) and ipsilateral common iliac blood flow were recorded simultaneously during REM sleep in rats. Furthermore, the lumbar sympathetic nerve was surgically sectioned unilaterally and in chronic studies the responses of the iliac blood flows in the innervated and denervated sides were compared to allow more clear evaluation of the contribution of LSNA in regulating muscle blood flow during REM sleep in rats.
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Methods |
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Male Wistar rats weighing 380 ± 10 g (mean ±S.E.M., n= 24) were used for all experiments. Rats were housed individually in a temperature (24°C), humidity (60%) and light (12 h:12 h light–dark cycle, light 7.00–19.00 h) controlled room. The animals were allowed standard laboratory rat chow and water ad libitum and handled every day. Rats were assigned randomly to two groups: (1) animals having intact lumbar sympathetic nerves (n= 13) with LSNA and the iliac blood flow to the ipsilateral hindquarter being measured; and (2) a second group which underwent unilateral lumbar sympathectomy (n= 11) with common iliac blood flows to both ipsilateral and contralateral hindquarters being recorded. All procedures were carried out in accordance with the Guiding Principles in the Care and Use of Animals in the Field of Physiological Sciences published by the Physiological Society of Japan and with the prior approval of the Animal Care Committee of Nara Women's University.
Surgical procedures
All animals were operated on in two stages using aseptic procedures in the operating room. During the first surgical procedure, in both intact and lumbar-sympathectomized rats, electroencephalogram (EEG), electrocardiogram (ECG) and electromyogram (EMG) electrodes were implanted. The rat was anaesthetized with pentobarbitone sodium (65 mg kg–1, I.P.) and placed in a stereotaxic head holder. EEG electrodes were implanted over the frontal cortex (anteroposterior +2 mm, mediolateral –2 mm from bregma), the parietal cortex (anteroposterior –3 mm, mediolateral –2 mm from bregma) and over the cerebellum (1.5 mm posterior to lambda). Three miniature stainless-steel screws (1.0 mm diameter), which served as electrodes, were screwed into the skull and secured with dental cement. Bipolar EMG electrodes were implanted bilaterally in the trapezius muscle. A bipolar EMG electrode was also implanted in the biceps femoris muscle of the left hindquarter to identify the exact point of the onset of moving behaviour. The bipolar ECG electrode was implanted under the skin at the manubrium of the sternum and xiphoid process. The electrodes were exteriorized at the back of the neck and passed through the centre of a circular Ducron sheet, which was fixed into place by suturing to the skin and protected by plastic tubes. After surgery, the animals were housed individually in transparent plastic cages and allowed standard laboratory rat chow and water ad libitum.
At least 5 days after the first surgery, the rats were again anaesthetized with pentobarbitone sodium and the electrodes for measurement of LSNA and a Doppler flow cuff for the measurement of the ipsilateral hindquarter blood flow were implanted. A mid-line abdominal incision was made and, after retraction of the intestines, the abdominal aorta and vena cava were gently pulled aside to expose a lumbar nerve. The left sympathetic trunk lies on the psoas muscle located under the aorta. Approximately 3 mm of the left lumbar sympathetic trunk was carefully isolated from the connective tissue. A piece of laboratory film (
2 x 3 mm; Parafilm, American National Can, Greenwich, CT, USA) was placed under the isolated nerve. The two tips of the electrodes (AS633, Cooner wire, Chatsworth, CA, USA) were hooked on the sympathetic trunk between L3 and L4 by placing the electrode between the sympathetic trunk and the film. The third electrode tip was placed between the film and the connective tissue and served as a grounding electrode. The LSNA was amplified using a differential amplifier (MK-2, Biotex, Kyoto, Japan), displayed on an oscilloscope and made audible with an audio amplifier. When optimal nerve activity was confirmed by observing the rhythmic bursts of nerve traffic, the wires of the electrode and the isolated sympathetic trunk were embedded in a two-component silicone gel (932, Wacker-chemie, Munich, Germany). Once the gel had hardened, the silicone rubber was fixed to the surrounding tissue using glue containing 
-cyano-acrylate (Aronalpha, Tohwa Gousei Kagaku, Tokyo, Japan). Subsequently, the left common iliac and the origin of the superior mesenteric arteries were freed for approximately 1 cm from the surrounding tissue, and Doppler flow cuffs (Iowa Doppler Products, Iowa City, IA, USA), were placed around the left common iliac and superior mesenteric arteries (Haywood et al. 1981). Finally, the arterial catheter was implanted into the abdominal aorta via the tail artery, and the venous catheter was implanted via the right internal jugular vein. The electrodes, probes and catheters were also tunnelled subcutaneously and then exteriorized at the back of the neck and protected by plastic tubes.
In a separate group of rats, a unilateral lumbar sympathectomy was carried out no earlier than 5 days after the first surgery. In pentobarbitone-anaesthetized rats, a mid-line abdominal incision was made, and the abdominal aorta and vena cava were gently pulled aside to expose the left lumbar sympathetic trunk. The left lumbar sympathetic trunk from L3 to L5 was cut and removed. Then the left and right common iliac arteries were isolated for approximately 1 cm from the surrounding tissue, and Doppler flow cuffs (Iowa Doppler Products, Iowa City, IA, USA) were placed around both left and right iliac arteries. Thereafter, the arterial catheter was implanted into the abdominal aorta via the tail artery, and the venous catheter was implanted via the right internal jugular vein. The electrode, probes and catheters were exteriorized as described above.
On completion of each surgery, antibiotics were given I.P. (Fradiomycin 200 µg kg–1, Mochida-Seiyaku, Tokyo, Japan). For the control of postoperative pain, a non-steroidal anti-inflammatory drug (diclofenac sodium, Voltaren; 0.5–3 mg kg–1, Novartis, Japan, Tokyo) mixed with jelly was given orally when necessary. The animals were housed individually in transparent plastic cages and then acclimated to the recording environment over the recovery period. The animals were weighed and handled every day, and the status of the animals was checked at least twice a day by experienced researchers. The arterial and venous catheters were filled with heparin sodium solution (1000 i.u. ml–1 saline) and were flushed every day.
Measurements
The EEG, ECG, EMG and LSNA signals were amplified by a differential amplifier (MK-2, Biotech, Kyoto: gain x10 000 and bandwidth 0.16–50 Hz for EEG; gain x1000 and bandwidth 0.16–150 Hz for ECG; gain x100 and bandwidth 100–2000 Hz for EMG; and gain x10 000 and bandwidth 150–2000 Hz for LSNA). The Doppler flow cuff was connected to a pulsed Doppler flow meter (PDV-20, Crystal Biotech, Northborough, MA, USA). Arterial and central venous pressures were measured by connecting the catheters to a pressure transducer (DX-100, Nihon Kohden, Tokyo, Japan). Physiological data were recorded simultaneously on a thermal-head paper recorder (ORP 1200, Yokogawa-Denki, Tokyo, Japan), a magnetic tape recorder (RX-8016, TEAC, Tokyo, Japan) and sampled at 1000 Hz using the 12 bit A/D converter of the computer. The digitized EEG was Fourier analysed continuously and simultaneously every 1 s using a data acquisition program (Visual Designer 4.0, Intelligent Instrumentation, Tucson, AZ, USA). EEG power density values were averaged in two frequency bands: delta (0.5–4.0 Hz) and theta (6.0–9.0 Hz) bands. Heart rate was determined with a cardiotachometer (AT-601G, Nihon Kohden, Tokyo, Japan) triggered by the ECG. The root mean square value of EMG was calculated simultaneously. The amplified LSNA was integrated using a voltage integrator (AD-600G, Nihon Kohden, Tokyo, Japan). The area of integrated nerve discharge was calculated simultaneously by means of the computer. The mean values of the data were calculated simultaneously and continuously displayed on the computer every 1 s, and stored on the hard disk.
Experimental protocols
Recordings were carried out in a sound-attenuated, temperature (24°C) and humidity (60%) controlled chamber (Espec, Osaka, Japan) not less than 3 days after the second surgery. The recording session was carried out between 10.00 am and 3.00 pm after an hour rest when all electrodes, probes and catheters had been connected to the measuring instruments. Each recording session lasted 1–2 h and was repeated two or three times per day. The animals were monitored visually by the investigator through a small acrylic window of the chamber throughout the recording session. The momentary active behaviour of each rat was noted at every second.
Following the final recording session of each day, the background noise of LSNA was determined when nerve activity was eliminated by increasing arterial pressure up to 170 mmHg with an intravenous infusion of phenylephrine (10 µg). The background noise was then subtracted from the integrated LSNA data.
At the end of the entire procedure, rats were humanely killed using an intravenous overdose of pentobarbitone sodium (>200 mg kg–1). The biceps femoris and soleus muscles were removed bilaterally and stored frozen (–40°C) for measurement of the tissue noradrenaline content. The noradrenaline concentration was measured using high-performance liquid chromatography coupled with trihydroxyindole fluorometry (Nagatu, 1973). Sympathectomy was verified by the marked reduction in noradrenaline content of the sympathectomized tissue.
Data analysis
Behavioural states were scored by standard criteria on the basis of EEG and EMG as well as behavioural observations noted at the time of data collection. The animal's behaviour was classified as REM, NREM, quiet awake, moving and grooming states (Miki et al. 2003). REM sleep was characterized by body relaxation, irregular breathing and muscle twitches in different parts of the body; the EEG was desynchronized and displayed low-voltage and high-frequency waves, with predominant EEG power density occurring within the theta frequency band, an elevated value of the theta:delta ratio and a dramatic suppression of the EMG. During NREM sleep, the animal lay immobile with eyes closed; the EEG was synchronized and displayed high-voltage low-frequency waves, with high-power density values in the delta frequency band. The quiet awake state was identified by a low-amplitude EEG with the animal maintaining a lying position with its eyes open. Moving and grooming behaviour was identified by the visual observation taken during data acquisition. Moving behaviour included any body movement except grooming, eating and drinking, for example stretching, exploring and rearing.
To quantify the LSNA response, percentage changes in nerve activity were calculated by comparing the value obtained in each behavioural state to the mean of the values during the NREM period, which were taken as 100% LSNA. Iliac vascular conductance was calculated by dividing iliac blood flow by the systemic pressure gradient (systemic arterial pressure minus central venous pressure).
Statistical analysis
Statistical analysis was performed using analysis of variance (ANOVA) for repeated measures. When the F-values were significant (P < 0.05), individual comparisons were made using Fisher's least significant difference test (Sachs, 1982). Dependencies between LSNA and the iliac vascular conductance were quantified using a least-squares linear regression (Sachs, 1982). To avoid the effects of uneven density of Y-axis data along the X-axis, all data for the dependency analysis were averaged over each 2% bin of iliac vascular conductance. Mean values of the iliac vascular conductance and LSNA within every 2% of the iliac vascular conductance were used for the regression analysis. Values are reported as means ±S.E.M.
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Results |
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The relationship between the changes in LSNA and iliac vascular conductance during the transition between NREM and REM sleep is shown in Fig. 6. There was a significant (P < 0.05) inverse linear relationship between LSNA and iliac vascular conductance.
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Tissue noradrenaline concentration measured post mortem in biceps femoris and soleus muscles of the innervated side was 28.15 ± 14.3 and 36.58 ± 27.27 ng g–1, respectively, whereas that of the denervated side was 1.42 ± 1.22 and 2.96 ± 2.63 ng g–1, respectively (P < 0.05 versus innervated side).
Figure 7 shows the effects of unilateral lumbar sympathectomy on the changes occurring in iliac blood flow and iliac vascular conductance during the transition between NREM and REM sleep. Iliac blood flow in the denervated side decreased transiently at the onset of REM sleep, from –12 to +13 s (Fig. 7, P < 0.05), and then it returned to the pre-REM level; thereafter this level was maintained throughout the period of REM sleep. By contrast, iliac blood flow in the innervated side decreased in a stepwise manner to a mean level of –1.3 ± 0.1 kHz (13 ± 1% relative to the pre-REM level, P < 0.05), which was maintained throughout the period of REM sleep. The change in iliac blood flow in the denervated side was significantly (P < 0.05) blunted compared with that in the innervated side over the period from –10 to +120 s (Fig. 7). The response of iliac vascular conductance observed in the denervated side to the onset of REM sleep was also blunted compared with that in the innervated side (P < 0.05, from –8 to +120 s, Fig. 7). Systemic arterial pressure in the unilaterally sympathectomized rats (Fig. 8) increased gradually but significantly (P < 0.05) from 17 s after onset of REM sleep, while central venous pressure remained constant and heart rate decreased in a stepwise manner, by –13.4 ± 3.9 beats min–1 (P < 0.05), during the transition from NREM to REM sleep.
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Discussion |
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Diverse changes in sympathetic nerve activity during REM sleep
Although LSNA and renal sympathetic nerve activity were not measured in the same animal, the responses in LSNA, in the present study, and renal sympathetic nerve activity to REM sleep, in our previous study, in the same species under the same experimental protocol, would allow us to conclude that the regulation of sympathetic outflow during REM sleep did not consist of a simple unidirectional readjustment. It is therefore likely that renal sympathoinhibition coexists with lumbar sympathoexcitation during REM sleep in rats. This view would be consistent with the observations of Futuro-Neto & Coote (1982) that reductions of renal, cardiac and splanchnic sympathetic nerve activities were observed whilst sympathetic activity to the gastrocnemius muscle increased during an REM sleep-like state induced by physostigmine in the decerebrated cat. To our knowledge, no other reports suggesting the existence of diverse changes in sympathetic outflow during REM sleep have been reported since the study by Futuro-Neto & Coote (1982). However, sympathetic outflow to different organs has been measured separately during REM sleep in humans and cats. In humans, muscle sympathetic outflow has been measured and was consistently found to increase during REM sleep (Hornyak et al. 1991; Okada et al. 1991; Somers et al. 1993). In cats, a reduction of renal sympathetic nerve activity during REM sleep has been reported from different laboratories (Baust et al. 1968; Iwamura et al. 1969). The apparent discrepancy between observations in humans and cats has not been clarified because it is impossible to measure renal sympathetic nerve activity during REM sleep in humans and no attempt has been made to measure the muscle sympathetic nerve activity during spontaneous REM sleep in cats. Accordingly, species differences have been pointed out as one possible reason for the difference between humans and cats. The rise in LSNA (Fig. 3) and reduction of renal sympathetic nerve activity (Miki et al. 2003) observed during REM sleep in the same species provides solid evidence for the divergent changes in sympathetic nerve activity occurring during REM sleep in rats, and this finding could help explain and reconcile the apparent species difference between humans and cats, and supports the arguments put forward by Futuro-Neto & Coote (1982).
Role of LSNA in regulating muscle vasomotor tone during REM sleep
Although the role of sympathetic nerve activity in the regulation of muscle blood flow has been studied extensively, its contribution remains unclear. For instance, an active vasodilator influence of sympathetic nerve activity on the muscle vasculature has been reported (Joyner & Halliwill, 2000), so it was uncertain whether the increase in sympathetic nerve activity would cause vasoconstriction or vasodilation in the muscle during REM sleep. To approach this issue, we designed two experimental protocols to study the role of sympathetic nerve activity in regulating muscle blood flow during REM sleep.
Firstly, changes in LSNA, muscle blood flow and pressure gradient (systemic arterial pressure minus central venous pressure) to the same muscle were measured simultaneously, which enabled a direct assessment of the relationship between changes in sympathetic nerve activity and vasomotor tone occurring during REM sleep at the same time within the same animal. Lumbar sympathetic nerve activity was measured between L3 and L4 in order to study the role of muscle sympathetic nerve activity in regulating vascular tone of the hindlimb in the present study. The validity of this approach is based on the following reasons. From the anatomical viewpoint, the major source of sympathetic preganglionic neurones that innervates preaortic ganglia, including coeliac, superior and inferior ganglia, is located from C8 to L3 (Janig, 1985; Strack et al. 1988). Indeed, the inferior mesenteric ganglia that provide the innervation for the colonic and pelvic organs originates from T13 to L2, while the neurones at L3 contribute less than 5% to the inferior mesenteric ganglia (Strack et al. 1988). Moreover, the pelvic splanchnic nerves arise from the L6–S1 segment. It is therefore likely that the lumbar sympathetic nerves between L3 and L4 probably contain only a small number of fibres which supply colon and pelvic organs, whereas the majority of fibres are likely to innervate muscle and skin. Since the muscle is the predominant organ of the hindlimb, it is reasonable to speculate that the lumbar sympathetic nerves between L3 and L4 mainly contain fibres which supply the muscle. In addition, the present experiments were carried out under constant ambient temperature and humidity, which was attained by the climatic chamber. As a consequence, we could not discriminate the nerve activity innervating the skin from the whole recording, but the contribution of skin sympathetic nerve to the recording is likely to be small and would remain constant throughout the period of experimentation. From a functional viewpoint, the lumbar sympathetic nerve has long been used to study the role of sympathetic nerves in regulating vascular tone of the hindlimb, for instance, in the early studies by Mellander (1960) in cats (L4) and in recent studies by Coney & Marshall (2003) in rats (L3–L4). Coney & Marshall (2003) have studied the role of sympathetic nerve in regulating muscle vascular tone by stimulation of the lumbar sympathetic nerve of rats at the L3–L4 segment during hypoxia, and they have provided consistent results. In the present study, denervation of the L3–L5 level reduced muscle noradrenaline concentration by some 90%. Together, these observations provide strong evidence to support the view that there is a functional linkage between the lumbar sympathetic nerve at L3–L4 and vascular tone of the hindlimb. Based on the above reasoning, we concluded that the lumbar sympathetic nerve activity between L3 and L4 provided an index of muscle sympathetic nerve activity of the hindlimb. As shown in Fig. 3, changes in LSNA were closely mirrored by changes in iliac vascular tone and there was a significant (P < 0.05) inverse linear relationship between LSNA and iliac vascular conductance. This suggests that LSNA is a likely cause of vasoconstriction of the hindlimb during REM sleep in rats.
Secondly, we attempted to support this view by evaluating the vascular responses subsequent to unilateral lumbar sympathectomy. This allowed comparison of the iliac blood flows when muscles had an intact sympathetic innervation with those following sympathectomy and measured simultaneously and continuously. This within-animal design ensured that each hindlimb was subjected to the same perfusion pressure and circulating levels of humoral factors, so any differences in responses in iliac blood flows and conductances could be attributed to the action of the sympathetic nerves. Unilateral lumbar sympathectomy prevented the ipsilateral reduction of iliac blood flow and blunted the fall in conductance compared with those in the contralateral hindquarter, indicating that the increase in LSNA exerted a vasoconstrictor action on the muscle vasculature, resulting in a decreased iliac blood flow during REM sleep. This view would be consistent with the previous report by Baccelli et al. (1974) in cats, in which REM sleep induced a long-lasting constriction of muscle blood vessels, which was abolished after sympathectomy. The present observations in rats and the previous report in cats suggest that the increase in LSNA is likely to exert a vasocontrictor influence on the hindquarter muscle vasculature.
Neural regulation of systemic arterial pressure during REM sleep
In the rat, we have confirmed that systemic arterial pressure increases during REM sleep (Sei & Morita, 1999). This could result from a reduction of the sympathetic outflow to the kidneys, possibly to the visceral organs and the heart, at the start of REM sleep (Futuro-Neto & Coote, 1982; Miki et al. 2003), causing the decrease in the vascular conductance of the kidney (Miki et al. 2002), the visceral organs and cardiac function. The reduction in heart rate (Fig. 5) may be explained in part by the reduction of sympathetic outflow to the heart (Futuro-Neto & Coote, 1982), which may cause a reduction of cardiac output. The decrease in vascular conductance of visceral organs (Fig. 4) and cardiac output would favour a decrease in systemic arterial pressure. However, if the increase in LSNA going to the hindquarter skeletal muscle causes a decrease in the muscle vascular conductance and the response of the conductance of the hindquarter muscle vascular bed is representative of other muscle vascular beds, a reduced muscle vascular conductance throughout the body may effectively balance the reductions in the vascular conductance of the visceral organs as well as cardiac output. Consequently, systemic arterial pressure may be increased during REM sleep.
The mechanisms underlying the non-uniform changes in sympathetic outflow which occurred during REM sleep are not evident from the present study. However, it should be noted that all measured parameters, including central (EEG), peripheral neural (LSNA and EMG) activities and cardiovascular variables (systemic arterial and venous pressures and heart rate), immediately returned to the pre-REM (NREN) level in a synchronized manner at the end of REM sleep (Figs 2–4, 5 and 7). This suggests, firstly, that modulation of those parameters during the transition from REM to NREM sleep could be caused by central mechanisms; it may possibly be related to the REM-on and REM-off neurones (Bentivoglio & Grassi-Zucconi, 1999). Secondly, the fact that systemic arterial pressure, heart rate and LSNA returned to pre-REM levels within 30 s after the end of REM sleep may suggest that the operating level of neural regulation of systemic arterial pressure might be set centrally in a state-specific manner, causing a functional dichotomy of systemic arterial pressure regulation during the transition between REM and NREM sleep. The present study provides a basis on which to address the issue of how the central mechanisms could elicit state-specific regulation of regional sympathetic nerve activities and systemic arterial pressure.
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ratio) and electromyogram (ECG) measured in the trapezius muscle and left hindquarter during the transitions from pre-REM (NREM) to REM and from REM to post-REM (NREM) periods
P < 0.05, significant difference from the averaged level obtained during the pre-REM period in the denervated side.