| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
-estradiol attenuate the exercise
pressor reflex in male cats
Departments of Internal Medicine and Human Physiology, Division of Cardiovascular Medicine, University of California, Davis, California 95616
 |
ABSTRACT |
|---|
 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Previously, intravenous injection
of 17
-estradiol in decerebrate male cats was found to attenuate
central command but not the exercise pressor reflex. This latter
finding was surprising because the dorsal horn, the spinal site
receiving synaptic input from thin-fiber muscle afferents, is known to
contain estrogen receptors. We were prompted, therefore, to reexamine
this issue. Instead of injecting 17-estradiol intravenously, we
applied it topically to the L7 and S1 spinal
cord of male decerebrate cats. We found that topical application
(150-200 µl) of 17-estradiol in concentrations of 0.01, 0.1, and 1 µg/ml had no effect on the exercise pressor reflex, whereas a
concentration of 10 µg/ml attenuated the reflex. We conclude that, in
male cats, estrogen can only attenuate the exercise pressor reflex in
concentrations that exceed the physiological level.
estrogen; neural control of circulation; thin fiber muscle afferents; control of breathing; spinal cord; dorsal horn
| |
INTRODUCTION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
RECENT STUDIES IN HUMANS have shown that the cardiovascular and sympathetic neural responses to a given level of exercise were less in premenopausal women than in either men or postmenopausal women (8, 9). Moreover, the cardiovascular responses to exercise were attenuated by administration of oral estrogen in postmenopausal women (22). This difference was attributed to the effects of estrogen on the two neural mechanisms controlling autonomic outflow. The first of the two mechanisms is central command, and it is defined as the parallel activation of the central neural circuits controlling autonomic, ventilatory, and motor function (7). Central command does not require feedback from exercising muscles (25). The second mechanism is the exercise pressor reflex, which arises from the contraction-induced stimulation of group III and IV muscle afferents (4, 15). The exercise pressor reflex is believed to be activated by both mechanical and metabolic factors arising in the contracting muscles (14).
In animals, investigators can easily examine the separate effects of central command and the exercise pressor reflex on the cardiovascular responses to exercise. Nevertheless, there is only one study that examined the effects of estrogen administration on these two neural mechanisms (12). This study found that, in decerebrate male cats, intravenous injection of estrogen attenuated central command but had no effect on the exercise pressor reflex (12). This finding surprised us because estrogen receptors have been reported to be located on many neurons in the dorsal horn of the spinal cord (2). Moreover, many of the neurons displaying receptors for estrogen are found in laminae of the dorsal horn that are known to receive synaptic input from group III and IV muscle afferents (5, 19).
These reports prompted us to reexamine the effect of estrogen on the exercise pressor reflex in decerebrate male cats. Instead of injecting this sex hormone intravenously, we applied it topically to the dorsal surface of the spinal cord. We reasoned that if estrogen had effects on the exercise pressor reflex it would be revealed by direct application to the spinal cord. We found that topical application of estrogen to the cord attenuated the pressor component of the exercise pressor reflex, but only when the concentration exceeded the physiological level.
| |
METHODS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Surgical preparation. Adult male cats (n = 33, average body weight = 3.9 ± 0.2 kg) were anesthetized initially with 5% halothane in oxygen. The trachea was cannulated, and the lungs were ventilated mechanically (Harvard Apparatus) with 2% halothane in oxygen. Catheters were placed in the right jugular vein and common carotid artery for delivery of drugs and for measurement of arterial blood pressure, respectively. The carotid artery catheter was connected to a pressure transducer (model P23 XL, Statham). Heart rate (HR) was calculated beat to beat from the arterial pressure pulse (Gould Biotach).
The cat was placed in a Kopf sterotaxic spinal unit and then given dexamethasone (4 mg iv). A midcollicular decerebration was performed, after which anesthesia was terminated. All neural tissue rostral to the section was removed. Bleeding was controlled, and the cranial vault was filled with agar (37°C). A laminectomy was performed to expose the lumbar and sacral spinal cord. The L7 or S1 ventral root was identified and cut. A well of vinylpolysiloxane (VPS; Jeneric/Pentron) was installed on the spinal cord and enclosed the L6 to S1 dorsal roots. The method has been described in detail elsewhere (3, 26). To ensure its integrity, the well was filled with saline and checked for leakage. The well was filled either with saline or drugs dissolved in saline or oil throughout the experiment. The skin of the back was used to form a space for a pool around the exposed parts of the spinal cord, including the VPS well; the pool was then filled with warm mineral oil (37°C). The saline-containing well, therefore, was seated in the mineral oil pool; this allowed us to continuously monitor the well for leaks. In some cases, the well was filled with fast green dye at the end of the protocol to reveal leakage into the surrounding tissue. Only data derived from cats in which no leakage was detected were analyzed. The musculature of the left hindlimb was exposed, and all visible branches of the sciatic nerve, except for those innervating the triceps surae muscles, were sectioned. The calcaneal bone was severed, and its tendon was attached to a force transducer (model FT 10, Grass Instruments). The knee and ankle were clamped in place. The cat was removed from the ventilator and was allowed to breathe room air spontaneously. Airflow was measured with a pneumotach (Fleisch) attached in series to the tracheal tube. Airflow was integrated (Gould) breath by breath to yield tidal volume, which was used to calculate minute ventilation (
E).
Protocols.
Static contractions were evoked by electrically stimulating the
L7 or S1 ventral root at two to three times
motor threshold (0.1 ms, 30-40 Hz). Resting tension of the triceps
surae muscles was set at 1.0 kg. The contraction period varied between
cats (30-60 s). Each cat underwent two to three static
contractions before drugs were administered into the VPS well. The time
between subsequent electrical stimulations was 15 min. 17-Estradiol, which was dissolved in mineral oil, was placed in the spinal VPS well
in concentrations of 0.01, 0.1, 1, or 10 µg/ml. The volume was
150-200 µl. In a previous study in rats (3), the
tissue concentration of neurokinin A [molecular weight (MW) of 1,133] in the underlying superficial laminae of the spinal cord (at a depth of
500 µm) was 25-70 times lower than the concentration in the
superfusate in the well. Peak concentration was reached after 30 min of
diffusion. The tissue concentration in the deeper laminae (depth of
0.75-1.5 mm) was found to be lower than that in the superficial
laminae (3). In cats, the GABA-blocker muscimol (MW:
114-195), which was applied in a similar manner to the dorsal root
of the spinal cord, was found to block the exercise pressor reflex
(26). Therefore, we choose our lowest dosage of estrogen (MW: 272) to be ~70 times the physiological estrogen concentration in
blood during peak estrus.
-estradiol previously placed in the well. Lidocaine, which has a
MW (i.e., 234) comparable to 17-estradiol (i.e., 272), was used as
control to assure that the diffusion of the applied concentration was
sufficient to reach the neurons that are involved in the exercise
pressor reflex arc. Moreover, both lidocaine and 17-estradiol are
hydrophobic. The similarities in both MW and solubility led us to
speculate that the two substances would have similar diffusion
properties within the spinal cord. Nevertheless, the threshold tissue
concentrations needed to cause an effect for the two substances might
be different.
Lidocaine was applied for 60-75 min. After 30 min, the response to
the muscle contraction was tested in 15-min intervals. In cats in which
we observed an obvious attenuation of the exercise pressor reflex by
estrogen, the well was flushed three times and then filled with saline
to determine whether the exercise pressor reflex would recover over a
2-h time period.
Data analysis.
Values for mean arterial pressure (MAP), HR, and E
are expressed as means ± SE. Baseline MAP and HR were recorded
immediately before muscle contraction; peak values represent the
highest level reached during the muscle contraction.
Ventilation was calculated as a minute volume immediately
before (baseline) and during the contraction ("peak").
| |
RESULTS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Effects of 17-estradiol on the pressor response to muscle
contraction.
17-Estradiol applied topically to the spinal cord in a concentration
of 10 µg/ml significantly attenuated the pressor response to
contraction of the triceps surae muscles (Fig. 1; Tables
1 and 2). The
pressor response was significantly
attenuated 45 min after estrogen
application (21 ± 6 mmHg; n = 13) compared with
the one before estrogen application (control, 32 ± 3 mmHg) (Fig.
2). In those cats (n = 7)
in which recovery from estrogen application was attempted, the
attenuating effect of 17-estradiol was found to be maintained for 90 min after the end of the application (Table 2). Baseline MAP did not
change over time for any of the concentrations of 17-estradiol
tested (Fig. 2).
|
|
|
|
-estradiol did
not attenuate the pressor response to muscle contraction (Table 2).
However, lidocaine applied in the same concentrations as 17-estradiol significantly reduced (P < 0.05) the
pressor response (Table 2). In three animals, in which no obvious
effect of 0.01 µg/ml lidocaine was detectable, 0.1 µg/ml lidocaine
was applied subsequently. An attenuating effect was observed at this
dosage; the effect in these cats, however, was not significant
(P > 0.05).
Effects of 17-estradiol on the cardioaccelerator response to
muscle contraction.
17-estradiol did not have any effect on the cardioaccelerator
response to muscle contraction in any of the concentrations tested
(Fig. 2; Table 3). Only at the 30- and
90-min time points of recovery after the 10 µg/ml 17-estradiol
treatment was the cardioaccelerator response significantly reduced
compared with the pretreatment value (Table 3). With one exception,
lidocaine at any of the concentrations tested did not attenuate the HR
response to muscle contraction. In three cats in which lidocaine at a
concentration of 0.01 µg/ml did not decrease the pressor response to
contraction, a subsequent application at a concentration of 0.1 µg/ml
attenuated the cardioaccelerator response. Over time, baseline HR
increased for each of the concentrations of 17-estradiol tested
(Figs. 1 and 2).
|
Effects of 17-estradiol on the ventilatory response to muscle
contraction.
There was no significant effect of either 17-estradiol or lidocaine
on the ventilatory response to muscle contraction at any of the
concentrations tested (Table 4; Fig. 2).
Baseline E was highly variable over time. After
application of either 10 or 1 µg/ml 17-estradiol, baseline
E increased significantly (P < 0.05), whereas at the lesser concentrations it did not change (Figs. 1
and 2).
|
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
In our experiments, only the highest concentration (i.e., 10 µg/ml) of 17-estradiol, topically applied to the spinal cord of
male decerebrate cats, attenuated the exercise pressor reflex. This
highest concentration was likely to create concentrations of
17-estradiol that exceeded physiological levels in the dorsal horn
of the spinal cord. Consequently, our present findings are consistent
with a previous one from this laboratory (12) that did not
observe an effect of intravenously injected 17-estradiol on the
exercise pressor reflex at concentrations of 0.01-1 µg/kg in
male decerebrate cats.
The possibility that the applied concentrations may not have been sufficient to stimulate estrogen receptors involved in the exercise pressor reflex arc can be excluded because the same concentrations of lidocaine, which is similar in MW to estrogen, attenuated the pressor response to muscle contraction. Nevertheless, we observed no obvious attenuating effect of the lowest concentration of lidocaine (i.e., 0.01 µg/ml) in three of the seven cats tested. We cannot exclude the possibility that this concentration of lidocaine failed to reach the target areas in these animals.
Our results question the origin of the attenuating effect of estrogen
on the exercise pressor reflex. The attenuating effect could have been
due to the effect of estrogen on other neural tissue to which it may
have been distributed by the bloodstream. In an experimental setup
similar to ours (e.g., the spinal VPS well) (3), one-third
of a radioisotope tested was reported to be absorbed into the blood.
Accordingly, a well filled with 200 µl of a 10 µg/ml estrogen
solution in our study translates into a concentration of 0.7 µg of
estrogen in the total blood volume of the cat. However, a blood-derived
effect at this concentration of estrogen in the blood can be excluded
because an even higher concentration of 17-estradiol (1 µg/kg)
administered intravenously had no effect on the exercise pressor reflex
(12). Therefore, the attenuation of the reflex by topical
application of estrogen to the spinal cord was probably due to an
effect in the dorsal horn.
When interpreting our results, we need to take into account that our study was done in male cats. Although use of males provides the advantage of a controlled estrogen level, this approach will not reveal potential sex-specific effects. Therefore, a sex-specific mechanism may account for the lack of an effect of estrogen at physiological dosages in our study. For example, female mice possess a sex-specific stress-induced non-opioid, non-NMDA analgesic mechanism. This female-specific system is known to be estrogen dependent (16, 17) because it disappeared after ovariectomy and was reinstated by estrogen replacement therapy. In contrast, estrogen treatment of intact or castrated males did not induce this analgesic effect, indicating an insensitivity of this system to estrogen in the male mouse (21). Quantitative trait locus mapping identified a female-specific locus on chromosome 8. This female-specific mechanism, which is sensitive to estrogen modulation, is consistent with a gene that is turned off by testosterone exposure during sexual differentiation (16, 17, 20). A similar sex-specific mechanism may be involved in the regulatory effect of estrogen on the exercise pressor reflex and may account for the lack of an effect at physiological dosages in the male animals.
A second example of a possible sex-specific effect concerns the
expression of calcitonin gene-related peptide (CGRP) in rat lumbar
dorsal root ganglion cells. Yang et al. (27) found that 17-estradiol inhibited the expression of CGRP in these cells. Specifically, ovariectomized rats treated with 17-estradiol had a
lower percentage of CGRP containing cells in the L3 dorsal
root ganglion than did ovariectomized rats that were not treated with the hormone. In addition, intact females had a lower percentage of
CGRP-containing cells than did ovariectomized females. These findings
lead us to speculate that, if CGRP functions as a neurotransmitter or
neuromodulator for primary afferents evoking the exercise pressor reflex, its lack of expression in females might be one reason that
premenopausal women exhibit a smaller reflex than men or postmenopausal
women (8, 9).
Our finding that a high concentration of estrogen attenuated the
exercise pressor reflex in male cats cannot be ignored. There are
indications in the literature that this attenuation might be caused by
an opioid mechanism. In cats, intrathecal administration of opioids
attenuated the exercise pressor reflex by stimulating µ and 
receptors (13). Furthermore, in ovariectomized rats, intrathecal injection of estrogen raised the nociceptive threshold by
activation of 
and opiate receptors (6).
Enkephalin-synthesizing neurons with intracellular estrogen receptors
have been identified in the superficial laminae of the spinal dorsal
horn (1). These neurons have been found to react to
estrogen with an acute increase in enkephalin mRNA expression,
suggesting that estrogen has an acute effect on spinal opioid levels.
In one study, however, subcutaneous injection of estrogen in
ovariectomized rats decreased pain sensitivity, but the effect could
not be explained by its effect on opioid receptors (11).
Finally, the expression of 
- and -estrogen receptor mRNA has been
shown to fluctuate with the estrogen levels in the estrous cycle
(23).
In contrast to the pressor response, estrogen applied topically to the spinal cord did not attenuate the cardioaccelerator or the ventilatory components of the exercise pressor reflex. This suggests that the neural pathways involved in those responses are not under estrogen control or that an estrogen effect was countered by a supraspinal mechanism. Lidocaine attenuated the pressor response significantly and also showed a tendency to decrease the cardioaccelerator responses to contraction at concentrations of 1 and 10 µg/ml. The observation that lidocaine affects the pressor and cardioaccelerator responses but not the ventilatory response parallels the results of previous investigations (15) and raises the possibility that the ventilatory response may be dominated by mechanisms other than the exercise pressor reflex (24).
In our experiments, both baseline HR and E increased
over time, whereas baseline MAP remained constant. We do not know
whether the increases in baseline HR and E were
caused by the first contraction or whether they occurred over time. In
any event, the upward shifts in baseline appear to be found in studies
in which decerebrate, laminectomized cats undergo hindlimb muscular contraction (10, 18). Specifically, the upward shift in
baseline HR has been attributed to the withdrawal of parasympathetic
input to the heart (18). It is important to point out that
the primary focus of our studies was to examine the effect of spinal
application of estrogen on the pressor response to static contraction.
The exercise pressor reflex, which is evoked by static contraction of
the hindlimb muscles in animal preparations, is widely believed to
influence MAP but to have minimal effects on HR and ventilation (14, 25). This is especially the case when the tension
developed by the triceps surae muscles is modest, which was the case in our studies because it averaged less than half of the maximum (e.g.,
Ref. 26).
In summary, we have found that, in male cats, topical application of
high, but not low, concentrations of 17-estradiol to the lumbosacral
spinal cord attenuated the exercise pressor reflex evoked by static
contraction of the triceps surae muscles. This high concentration of
estrogen, in all probability, created spinal concentrations of the
hormone that exceeded the physiological level. Consequently, it seems
reasonable to conclude that, in male cats, estrogen in physiological
concentrations has no effect on the exercise pressor reflex. Whether
this proves to be the case in female cats (i.e., is a sex-specific
effect) remains to be determined.
| |
ACKNOWLEDGEMENTS |
|---|
We thank Angela DiStefano and Todd Heller for technical assistance.
| |
FOOTNOTES |
|---|
This work was supported by National Heart, Lung, and Blood Institute Grant HL-64125.
Address for reprint requests and other correspondence: P. M. Schmitt, TB 172, Univ. of California, Davis, CA 95616.
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.
First published December 6, 2002;10.1152/japplphysiol.00825.2002
Received 11 September 2002; accepted in final form 3 December 2002.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Amandusson, A,
Hallbeck M,
Hallbeck AL,
Hermanson O,
and
Blomqvist A.
Estrogen-induced alterations of spinal cord enkephalin gene expression.
Pain
83:
243-248,
1999.
2.
Amandusson, A,
Hermanson O,
and
Blomqvist A.
Estrogen receptor-like immunoreactivity in the medullary and spinal dorsal horn of the female rat.
Neurosci Lett
196:
25-28,
1995.
3.
Beck, H,
Schrock H,
and
Sandkuhler J.
Controlled superfusion of the rat spinal cord for studying non-synaptic transmission: an autoradiographic analysis.
J Neurosci Methods
58:
193-202,
1995.
4.
Coote, JH,
Hilton SM,
and
Perez-Gonzalez JF.
The reflex nature of the pressor response to muscular exercise.
J Physiol
215:
789-804,
1971.
5.
Craig, AD,
and
Mense S.
The distribution of afferent fibers from the gastrocnemius-soleus muscle in the dorsal horn of the cat as revealed by the transport of horseradish peroxidase.
Neurosci Lett
41:
233-238,
1983.
6.
Dawson-Basoa, ME,
and
Gintzler AR.
Estrogen and progesterone activate spinal kappa-opiate receptor analgesic mechanisms.
Pain
64:
607-615,
1996.
7.
Eldridge, FL,
Millhorn DE,
Kiley JP,
and
Waldrop TG.
Stimulation by central command of locomotion, respiration and circulation during exercise.
Respir Physiol
59:
313-337,
1985.
8.
Ettinger, S,
Silber DH,
Collins BG,
Gray KS,
Sutliff G,
Whisler SK,
McClain JM,
Smith MB,
Yang QX,
and
Sinoway LI.
Influences of gender on sympathetic nerve responses to static exercise.
J Appl Physiol
80:
245-251,
1996.
9.
Ettinger, SM,
Silber DH,
Gray KS,
Smith MB,
Yang QX,
Kunselman AR,
and
Sinoway LI.
Effects of the ovarian cycle on sympathetic neural outflow during static exercise.
J Appl Physiol
85:
2075-2081,
1998.
10.
Gelsema, AJ,
De Groot G,
and
Bouman LN.
Instantaneous cardiac acceleration in the cat elicited by peripheral nerve stimulation.
J Appl Physiol
55:
703-710,
1983.
11.
Gordon, FT,
and
Soliman MR.
The effects of estradiol and progesterone on pain sensitivity and brain opioid receptors in ovariectomized rats.
Horm Behav
30:
244-250,
1996.
12.
Hayes, SG,
Moya del Pino NB,
and
Kaufman MP.
Estrogen attenuates the cardiovascular and ventilatory responses to central command in cats.
J Appl Physiol
92:
1635-1641,
2002.
13.
Hill, JM,
and
Kaufman MP.
Attenuation of reflex pressor and ventilatory responses to static muscular contraction by intrathecal opioids.
J Appl Physiol
68:
2466-2472,
1990.
14.
Kaufman, MP,
and
Forster HV.
Reflexes controlling circulatory, ventilatory and airway responses to exercise.
In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc, 1996, p. 381-447, sect. 12, chapt. 10.
15.
McCloskey, DI,
and
Mitchell JH.
Reflex cardiovascular and respiratory responses originating in exercising muscle.
J Physiol
224:
173-186,
1972.
16.
McEwen, BS.
The molecular and neuroanatomical basis for estrogen effects in the central nervous system.
J Clin Endocrinol Metab
84:
1790-1797,
1999.
17.
McEwen, BS,
and
Alves SE.
Estrogen actions in the central nervous system.
Endocr Rev
20:
279-307,
1999.
18.
McMahon, SE,
and
McWilliam PN.
Changes in R-R interval at the start of muscle contraction in the decerebrate cat.
J Physiol
447:
549-562,
1992.
19.
Mense, S,
and
Craig ADI
Spinal and supraspinal terminations of primary afferent fibers from the gastrocnemius-soleus muscle in the cat.
Neuroscience
26:
1023-1035,
1988.
20.
Mogil, JS,
Richards SP,
O'Toole LA,
Helms ML,
Mitchell SR,
Kest B,
and
Belknap JK.
Identification of a sex-specific quantitative trait locus mediating non-opioid stress-induced analgesia in female mice.
J Neurosci
17:
7995-8002,
1997.
21.
Mogil, JS,
Sternberg WF,
Kest B,
Marek P,
and
Liebeskind JC.
Sex differences in the antagonism of swim stress-induced analgesia: effects of gonadectomy and estrogen replacement.
Pain
53:
17-25,
1993.
22.
Pines, A,
Fisman EZ,
Shapira I,
Drory Y,
Weiss A,
Eckstein N,
Levo Y,
Averbuch M,
Motro M,
Rotmensch HH,
and
Ayalon D.
Exercise echocardiography in postmenopausal hormone users with mild systemic hypertension.
Am J Cardiol
78:
1385-1389,
1996.
23.
Taleghany, N,
Sarjari S,
DonCarlos LL,
Gollapudi L,
and
Oblinger MM.
Differential expression of estrogen receptor alpha and beta in rat dorsal root ganglion neurons.
Neurosci Res
57:
603-615,
1999.
24.
Victor, RG,
Pryor SL,
Secher NH,
and
Mitchell JH.
Effects of partial neuromuscular blockade on sympathetic nerve responses to static exercise in humans.
Circ Res
65:
468-476,
1989.
25.
Waldrop, TG,
Eldridge FL,
Iwamoto GA,
and
Mitchell JH.
Central neural control of respiration and circulation during exercise.
In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc, 1996, p. 333-380, sect. 12, chapt. 9.
26.
Wilson, LB.
Dorsal horn administration of muscimol abolishes the muscle pressor reflex.
J Appl Physiol
90:
919-925,
2001.
27.
Yang, Y,
Ozawa H,
Lu H,
Yuri K,
Hayashi S,
Nihonyanagi K,
and
Kawata M.
Immunocytochemical analysis of sex differences in calcitonin gene-related peptide in the rat dorsal root ganglion, with special reference to estrogen and its receptor.
Brain Res
791:
35-42,
1998.
This article has been cited by other articles:
|
|
 |
|
  S. W. Wong, D. S. Kimmerly, N. Masse, R. S. Menon, D. F. Cechetto, and J. K. Shoemaker Sex differences in forebrain and cardiovagal responses at the onset of isometric handgrip exercise: a retrospective fMRI study J Appl Physiol, October 1, 2007; 103(4): 1402 - 1411. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. M. Schmitt, K. Gohil, and M. P. Kaufman Spinal estrogen attenuates the exercise pressor reflex but has little effect on the expression of genes regulating neurotransmitters in the dorsal root ganglia J Appl Physiol, March 1, 2006; 100(3): 958 - 964. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. M. Schmitt and M. P. Kaufman Estrogen's attenuating effect on the exercise pressor reflex is more opioid dependent in gonadally intact than in ovariectomized female cats J Appl Physiol, February 1, 2005; 98(2): 633 - 639. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. M. Schmitt and M. P. Kaufman Estrogen attenuates the exercise pressor reflex in female cats J Appl Physiol, October 1, 2003; 95(4): 1418 - 1424. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
