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Departments of Obstetrics and Gynecology, Harbor University of California Los Angeles Medical Center, David Geffen School of Medicine at University of California at Los Angeles, Torrance, California 90502
Submitted 24 February 2003; accepted in final form 28 March 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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; Qian
1986). Sympathoinhibition and widespread vasodilation are induced
by low-frequency transcutaneous nerve stimulation
(Kaada 1982;
Kaada and Eieben 1983) and EA
stimulation of Zusanli (ST36) in human
(Ernst and Lee 1986). Depressor
effects are also produced by EA applied to acupuncture points (acupoints) in
spontaneous hypertensive rats (Utsunomiya
et al. 1987) and in norepinephrine (NE)-induced hypertensive rats
(Lin and Li 1981). Han et al.
(1986) have demonstrated that
analgesic effect of EA is mediated by opioid peptides in the periaqueductal
gray. The sympathoinhibition induced by low-frequency EA-like stimulation is
not antagonized by noloxone, an opioid-receptor-blocking drug
(Kaada 1982;
Kaada and Eieben 1983). It has
been suggested that activation of somatic afferents and acupuncture
stimulation might modulate intestinal motility and cardiovascular responses
via somatosympathetic reflex (Sato et al.
1992,
1993). However, the neural
pathways and neurotransmitters responsible for the cardiovascular effects of
EA ST36 are unclear. It has been demonstrated that nitric oxide (NO) plays an
important role in the central regulation of sympathetic tone and mediates
tonic inhibition of renal sympathetic nerve activity and arterial blood
pressure (Ma and Long 1991;
Ma et al. 1995;
Sakuma et al. 1992). NO in the
brain stem plays an inhibitory role in the central modulation of somatocardiac
sympathetic C-reflex (Li et al.
1995).
The somatotopic organization of the gracile nucleus receiving peripheral
somatosensory afferents from the hindlimb has been demonstrated with
electrophysiological mapping studies and anterograde axons tracing techniques
in various mammals (Cliffer et al.
1992; Leem et al.
1994; Ueyama et al.
1994). The neurons in the gracile nucleus are activated by
peripheral nociceptive stimulation of the sciatic nerve
(Leem et al. 1994;
Ueyama et al. 1994). Previous
studies have shown that neurons in the gracile nucleus which receive
somatosensory afferent inputs originating in nociceptors project to the
thalamus (Cliffer et al. 1992;
Leem et al. 1994). A number of
recent studies have suggested that gracile nucleus is an integration center
for cutaneous and visceral information flowing into the thalamus, which plays
an important role in somatic and visceral pain processing (Al-Chaer et al.
1996a,b,
1997).
Previous studies have demonstrated that stimulation of the somatic sensory
nerve results in changes in sympathetic nerve activity and arterial blood
pressure (Cliffer et al. 1992;
Samso et al. 1994). Our recent
studies have found that NO in the gracile nucleus plays an inhibitory role in
cardiovascular responses to stimulus-evoked somatosympathetic reflexes (SSR)
in rats (Chen and Ma 2002).
Neuronal NO synthase (nNOS) immunoreactivity is enhanced in the gracile
nucleus by EA applied to the hindlimb acupoints
(Ma and Li 2002). The purpose
of the present study was to determine the role of the gracile nucleus in the
cardiovascular responses evoked by electrical stimulation of hindlimb
acupoint, ST36. The effects of L-arginine-derived NO synthesis in
the gracile nucleus on the cardiovascular responses to EA stimulation of ST36
were examined by microinjections of L-arginine and nNOS antisense
oligodeoxynucleotides (olidos) into the area.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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All experiments were performed using adult (5–8 mo) male
Sprague-Dawley rats. The protocol was approved by the Harbor–UCLA Animal
Care and Use Review Committee and was in accord with AAALAC and National
Institutes of Health guidelines. The animals were maintained on a 12-h
light:dark cycle in temperature- and humidity-controlled rooms. Food and water
were available ad libitum. The rats were anesthetized by an intraperitoneal
injection of urethan (1.3 g/kg), which maintained a stable anesthesia
throughout surgery, microinjections, and EA stimulations as previously
described (Ma and Long 1991;
Ma et al. 1995;
Chen and Ma 2002). Femoral
venous cannulae were implanted for systemic delivery of drugs. The femoral
arterial catheter was connected for recording arterial blood pressure and
heart rate. Polyethylene catheters (PE 50) filled with heparinized saline were
inserted into the right femoral artery for recording systemic arterial blood
pressure. Heart rate was monitored by a tachograph (Grass 7P4H) triggered by
the arterial blood pressure wave. After tracheal cannulation, the animals
breathed spontaneously throughout the experiment. A heating pad was used to
maintain body temperature at 37°C.
Electroacupuncture stimulation
EA was applied at the pairs of acupuncture points Zusanli (ST36) in rats
anesthetized by urethan as described above. The needle electrodes (27-gauge
sharpened stainless-steel insect pins) were inserted percutaneously into a
depth of 2–4 mm (cutaneous and muscle) at the points of ST36, at the
depression below the knee from the anterior crest of the tibia
(Ernst and Lee 1986;
Lee and Beitz 1993). EA
stimulation was performed using a Grass S48 stimulator connected to each pair
of needle electrodes. Biphasic pulse electrical stimuli with three frequencies
3, 10, and 30 pulses/s were applied to the acupoints. As previously described,
the parameters of stimulation were high-intensity stimuli (6 V, duration 1.0
ms) to activate the A
/A
and C fibers
(Han et al. 1986;
Ku et al. 1993;
Lee and Beitz 1993;
Wang et al. 1994). As a
control for the specific acupoint effects, stimulation using the same
parameters were applied to the "nonacupoints" located nearby ST36
in the hamstring muscles as described (Lee
and Beitz 1993).
Microinjection in the gracile nucleus
Rats were placed in a stereotaxic apparatus with the head flexed at 45°
to facilitate exposure of the obex. The dorsal surfaces of the medulla
oblongata were exposed through removal of a small section of the posterior
cranium and the area postrema was visualized under a microscope. Bilateral
microinjections were made into the gracile nucleus at approximately 1.0 mm
posterior to the calamus scriptorius, 0.5–1.0 mm lateral from midline
and at a depth of 0.5 mm to the surface of the medulla
(Leem et al. 1994;
Ma and Long 1991).
Single-barrel glass cannula (1.14 mm OD and 0.5 mm ID, World Precision) were
pulled; the outer tip diameter was approximately 50 µm. The cannula was
connected to an electronically controlled nano-liter injector (A203XVZ, World
Precision). Agents were dissolved in artificial cerebral spinal fluid (pH
adjusted to 7.4) and were given in a volume of 50 nl over a period of 5 s.
To identify the site of microinjection, 2% pontamine sky blue was injected
into the gracile nucleus when the experiment was completed. The animals were
deeply anesthetized; the brains were removed and stored in 10%
paraformaldehyde solution. The frozen brain tissue was sectioned in the
coronal plane (40 µm). Histological verification was carried out with
reference to the rat brain in stereotaxic coordinates
(Paxinos and Watson 1997). The
stained area in the brain stem containing the gracile nucleus was examined
under a light microscope. The results from the animals with injections
diffusing out of the gracile nucleus were excluded from statistical data.
Protocol
The rats were randomly divided into five groups. Arterial blood pressure
and heart rate were monitored and allowed to stabilize for 
20 min.
Cardiovascular responses were induced by EA stimulation of ST36 using 6 V with
a duration of 1.0 ms at 3, 10, 30 pulse/s for 10 s in random order in the same
rat. Frequency-response curves were obtained for the changes in arterial blood
pressure and heart rate induced by each stimulation at intervals of 5–7
min, to ensure that arterial blood pressure was completely maintained to the
baseline level. Lidocaine (10 µmol), L-arginine (3 nmol) versus
vehicle (same volume), were microinjected into the gracile nucleus. Before and
after administration of each compound into the gracile nucleus, arterial blood
pressure and heart rate were observed following EA stimulation of ST36.
Cardiovascular responses to ST36 stimulation in two additional groups of rats were examined by the presence of nNOS antisense oligos to block local NO generation in the gracile nucleus. nNOS antisense and sense oligos were designed and synthesized by Biognostik (Chemi-Con, Temecula, CA) based on rat nNOS gene sequence. nNOS sense or antisense oligos were dissolved in artificial cerebral spinal fluid (pH adjusted to 7.4) and given in a volume of 50 nl over a period of 30 s. After cardiovascular effects were obtained by EA stimulation of ST36, nNOS sense or antisense oligos (20 pmol) were microinjected bilaterally into gracile nucleus. Arterial blood pressure and heart rate were monitored for 2 h. The cardiovascular responses to EA ST36 were measured at 10-min intervals before and 15, 30, 45, 60, and 90 min after injection of sense and antisense oligos. Time-response curves of nNOS sense or antisense oligos in the gracile nucleus were obtained for the changes in arterial blood pressure and heart rate induced by EA stimulation of ST36.
Data analysis
Results are expressed as mean ± SE. Mean arterial pressure (MAP) and heart rate are presented using mmHg and beats per minute, respectively. Heart rate and changes in MAP were obtained by measurement of a peak response to each EA stimulation from baseline values. The effects of central pretreatments on EA responses are expressed as changes in MAP and heart rate was induced by EA stimulation as compared with control values. Two-way ANOVA and Fisher's least significant differences were used to analyze significant difference. P values <0.05 were considered significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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In rats anesthetized with urethan, EA stimulation of ST36 produced decreases in MAP and heart rate but the same stimulation on the nonacupoints caused slight cardiovascular responses (Fig. 1). The cardiovascular responses to EA ST36 were initiated within 15–30 s and lasted 2–3 min after a stimulation of 10 s. Figure 2 shows cardiovascular responses to EA stimulation of ST36 with three different frequencies. Frequency-dependent depressor and bradycardia were elicited by EA stimulation of ST36. Immediately following EA stimulation of ST36 with the highest frequency (30 pulse/s), decreases in MAP and heart rate were 16 ± 1 mmHg and 49 ± 4 beats/min. For the same stimulation on the nonacupoints, decreases in MAP and heart rate were 2 ± 1 mmHg and 5 ± 1 beats/min, much lower than the responses induced by EA ST36 (n = 7, P < 0.05). MAP and heart rate were not significantly altered by stimulation of nonacupoints compared with baseline values.
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To determine the roles of gracile nucleus in mediating the effect of ST36 stimulation, lidocaine (10 µmol) was injected bilaterally into the nucleus. The baseline of the MAP is 109.1 ± 1.9 mmHg and the mean heart rate is 343 ± 6 beats/min. Lidocaine in the gracile nucleus did not alter the baseline of MAP and heart rate. Following microinjection of lidocaine into gracile nucleus, hypotensive and bradycardiac responses to EA stimulation of ST36 were significantly blocked at all of the three different frequencies (n = 7, Fig. 2).
L-arginine microinjected into the gracile nucleus
To determine the effects of L-arginine in the gracile nucleus on the cardiovascular responses to EA stimulation of ST36, L-arginine (3 nmol) and vehicle were injected into the gracile nucleus (n = 5). The basal MAP and heart rate in rats were 108.1 ± 1.8 mmHg and 323 ± 5 beats/min, respectively. After microinjection of L-arginine into the gracile nucleus, the MAP was 105.3 ± 1.2 mmHg, and the mean heart rate was 331 ± 12 beats/min. The baselines of MAP and heart rate were not altered by microinjection of L-arginine or vehicle into the gracile nucleus. The frequency-dependent hypotensive and bradycardiac responses to ST36 stimulation were significantly enhanced by the presence of L-arginine in the gracile nucleus, as shown in Fig. 3. The responses to L-arginine on ST36 stimulation occurred 2–5 min after drug administration and lasted for 10–15 min, and the responses reversed at 20 min after the injection. Administration of vehicle has no effect on the cardiovascular responses to EA stimulation of ST36.
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nNOS antisense oligos microinjected into the gracile nucleus
The basal MAP and heart rate were 100.3 ± 2.6 mmHg and 328 ± 8 beats/min. Bilateral microinjection of antisense oligo into gracile nucleus did not alter the baseline of MAP and heart rate. After microinjection of antisense oligo into the gracile nucleus, the MAP is 97.1 ± 1.8 mmHg and heart rate is 339 ± 15 beats/min. Figure 4 shows the time-course reduction in cardiovascular responses to EA stimulation of ST36 by microinjection of nNOS antisense oligos in the gracile nucleus (n = 5). The hypotensive and bradycardiac responses to EA ST36 were significantly inhibited at 30, 45, and 60 min after the injection (P < 0.05). The maximum inhibitory responses occurred at 45 min and the responses reversed at 90 min after the injection. The EA ST36-evoked responses were not altered by injection of nNOS sense oligos into the gracile nucleus (n = 5, Fig. 4). Figure 5 presents a medullary coronal section summarizing the locations of gracile nucleus sites for microinjection during cardiovascular studies.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Acupuncture has long been used for the treatment of a wide spectrum of
cardiovascular diseases and diseases with hypertensive syndromes
(Ernst and Lee 1986;
Lin and Li 1981;
Qian 1986). The therapeutic
effects of EA have been studied in various animal experiments. Ohsawa et al.
(1995) demonstrated that
arterial blood pressure and sympathetic nerve activity were decreased by
acupuncture-like stimulation with frequency of about 1 Hz to hindlimb in
anesthetized rats. In nonanesthetized spontaneously hypertensive rats,
stimulation of somatic afferents in the sciatic nerve to mimic EA caused a
decrease in arterial blood pressure (Yao
et al. 1982). Our results are consistent with these reports and
demonstrate that a somatosympathetic pathway is involved in the mechanism of
EA ST36 elicited cardiovascular responses.
The gracile nucleus receives peripheral somatosensory nociceptive inputs
that trigger the SSR (Cliffer et al.
1992; Samso et al.
1994). Recently, a number of reports have suggested that the
gracile nucleus is an integration center for cutaneous and visceral
information flowing into the thalamus, which plays an important role in
somatic and visceral pain processing (Al-Chaer et al.
1996a,b,
1997). Our recent studies have
demonstrated that the L-arginine-derived NO synthesis in the
gracile nucleus facilitates the cardiovascular responses to stimulus-evoked
inhibitory SSR and attenuates the responses to excitatory SSR
(Chen and Ma 2002). Lidocaine
(lignocaine) is a local anesthetic that reduces the conductance of the
Na+ channel, and the excitatory transmitter release
(Kaneda et al. 1989). It has
been reported that intrathecally administered lidocaine can eliminate the
A-
and C fiber SSR evoked by the electrical stimulation of the tibial
and radial nerves (Wang et al.
1994). In our study, the inhibitory cardiovascular responses to EA
stimulation of ST36 are blocked by microinjection of lidocaine into the
gracile nucleus. These results support the previous concept that the
cardiovascular responses to SSR is inhibited by NO in the gracile nucleus
(Chen and Ma 2002) and further
suggest that the gracile nucleus plays an important role in the SSR neural
pathway mediating cardiovascular activities elicited by EA ST36. The results
also agree with the investigators who have reported that the gracile nucleus
is an important site in autonomic regulation through interaction of peripheral
somatosensory information with central pathways.
NO is an important diffusible neurotransmitter, which produces many
biological functions in the brain, and NO in the brain plays an important role
in the central regulation of cardiovascular responses. Recent studies have
demonstrated that the depressor effect of EA ST36 on hypertensive rats can be
reduced by microinjection of NO blocker into ventral periaqueductal gray
matter (Li et al. 2001).
NOS-positive neurons are distributed from the Zusanli point projecting to the
ganglia of L4 to S1 (Xiong et al.
1998). Jang et al.
(2003) showed that nNOS
expression is increased in periaqueductal gray area of rats with
streptozotocin-induced diabetes and acupuncture stimulation of ST36 suppressed
the diabetic enhancement in the nNOS expression. Our recent studies revealed
that EA stimulation of the cutaneous hindlimb acupoints induces nNOS
expression in the gracile nucleus of SD rats, which may contribute to
therapeutic effects of acupuncture (Ma and
Li 2002). It seems that EA-induced nNOS expressions may vary in
different brain areas and may be different from diabetic rats compared with
normal rats. The results of the present study showed that microinjection of
L-arginine into the gracile nucleus enhanced the depressor and
bradycardiac responses to EA stimulation of ST36. It is well known that NO is
synthesized from L-arginine catalyzed by nNOS in neurons. The data
suggest that L-arginine is transferred into NO, and the newly
formed NO produces inhibitory regulation of EA ST36 functions in the gracile
nucleus.
Recent studies demonstrated that neuronal gene expression in the brain can
be selectively blocked in vivo using antisense oligonucleotides complementary
to strategically chosen sequences within the target mRNA
(Maeda et al. 1999;
Neckers and Whitesell 1993).
It was reported that microinjection of nNOS antisense oligos into NTS produces
decreases in MAP and heart rate (Maeda et
al. 1999). The present results show that microinjection of nNOS
antisense oligos into the gracile nucleus attenuates the cardiovascular
responses to EA ST36. The changes started 30 min after the administration of
nNOS antisense oligos. The largest responses during the observation occurred
at 45 min after the injection and lasted 60 min. The time responses of our
studies are similar to the effects of microinjection of the nNOS antisense
oligos into the brain stem nuclei (Chen and
Ma 2002; Maeda et al.
1999). The results suggest the suppression of nNOS gene in the
gracile nucleus modify the cardiovascular response to EA ST36.
In summary, EA ST36 produces depressor and bradycardia and the effects are blocked by the presence of lidocaine in the gracile nucleus. L-arginine and suppression of nNOS gene in the gracile nucleus affect the inhibitory cardiovascular responses to EA ST36. We conclude that L-arginine-derived NO in the gracile nucleus contributes to central cardiovascular responses to EA ST36.
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DISCLOSURES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests: S.-X. Ma, Department of Obstetrics and Gynecology, Harbor-UCLA Medical Center, David Geffen School of Medicine at University of California at Los Angeles, 1124 W. Carson Street, RB-1, Torrance, CA 90502 (E-mail: ma{at}humc.edu).
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