| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Physiology, The University of Arizona Health Sciences Center, Tucson, Arizona 85721-0093
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Mateika, J. H., and R. F. Fregosi. Long-term
facilitation of upper airway muscle activities in vagotomized and
vagally intact cats. J. Appl. Physiol.
82(2): 419-425, 1997.
The primary purpose of the present
investigation was to determine whether long-term facilitation (LTF) of
upper airway muscle activities occurs in vagotomized and vagally intact
cats. Tidal volume and diaphragm, genioglossus, and nasal dilator
muscle activities were recorded before, during, and after one carotid
sinus nerve was stimulated five times with 2-min trains of constant
current. Sixty minutes after stimulation, nasal dilator and
genioglossus muscle activities were significantly greater than control
in the vagotomized cats but not in the vagally intact cats. Tidal
volume recorded from the vagotomized and vagally intact cats was
significantly greater than control during the poststimulation period.
In contrast, diaphragm activities were not significantly elevated in
the poststimulation period in either group of animals. We conclude that
1) LTF of genioglossus and nasal
dilator muscle activities can be evoked in vagotomized cats;
2) vagal mechanisms inhibit LTF in
upper airway muscles; and 3) LTF can
be evoked in accessory inspiratory muscles because LTF of inspired
tidal volume was greater than LTF of diaphragm activity.
vagal inhibitory memory; carotid sinus nerve; nasal dilator muscle; genioglossus muscle
INTRODUCTION LONG-LASTING ENHANCEMENT of ventilation, which is
observed for up to 90 min after stimulation of the carotid bodies or
carotid sinus nerve, is often referred to as long-term facilitation
(LTF). LTF of ventilation and of phrenic and inspiratory intercostal nerve activities has been well documented in cats (6, 14, 15) and other
animals (3, 8). However, few studies have examined LTF in upper airway
motoneuron pools, and the results obtained have been variable. Jiang et
al. (10) demonstrated that LTF of hypoglossal nerve activities is not
present in decerebrate/decerebellate cats, whereas Bach and Mitchell
(1) demonstrated LTF of hypoglossal nerve activity in intact rats.
Although species differences might account for the variable results, it
is possible that the absence of LTF in cat hypoglossal motoneurons was
due to decerebellation of the animals, since Hayashi et al. (8) showed
that LTF of phrenic nerve activities can be abolished in the rat after
removal of the cerebellum. Therefore, LTF of upper airway motor
activities may occur in the cerebellum-intact cat. Long-lasting
facilitation of upper airway dilator muscles would be of functional
significance because they play an important role in modulating upper
airway flow resistance (2, 17, 18). Therefore, the first purpose of
this investigation was to determine whether episodic carotid sinus
nerve stimulation evokes LTF in the genioglossus and nasal dilator
muscles of vagotomized, cerebellum-intact, spontaneously breathing
cats.
The second purpose of this investigation was to evaluate the role of
vagal afferents in the development and expression of LTF. To date, LTF
of ventilation and of phrenic and hypoglossal nerve activities has been
demonstrated primarily in vagotomized animals. It is conceivable that
the degree of LTF observed in vagotomized animals might be reduced in
intact animals by a long-lasting inhibitory memory, which could be
elicited by repeated stimulation of lung stretch receptors, which would
occur secondarily to the large tidal volume
(VT) changes that accompany
each episode of carotid sinus nerve stimulation. This hypothesis is
viable given that the activities of motor nerves innervating the nasal
dilator, genioglossus, and diaphragm muscles are reduced in response to lung inflations (2, 9, 12) and increased when lung inflation is
prevented in anesthetized vagally intact animals (16, 19). Furthermore,
Xi et al. (21) reported that short-term potentiation of ventilation
after exposure to hypoxia was significantly greater in dogs after their
vagus nerves were cooled. Similarly, Gesell and Hamilton (7) showed
that short-term facilitation of the phrenic nerve, which was elicited
by stimulating the saphenous nerve, was obscured when the vagi were
stimulated simultaneously. Despite this supporting evidence, no
investigation has been designed to determine whether a long-lasting
inhibitory vagal memory is evoked as a consequence of the increased
VT that accompany repeated episodes of carotid sinus nerve stimulation. Therefore, the second purpose of this investigation was to determine whether LTF, induced by
carotid sinus nerve stimulation, is attenuated in animals with intact
vagus nerves.
METHODS
-chloralose (35-50 mg/kg) and urethan (200 mg/kg) was
administered intravenously. We ensured that an effective analgesic level was maintained throughout the transition by monitoring the withdrawal and pupillary reflexes of the animal.
P < 0.05.
A one-way analysis of variance with repeated measures was used to determine whether a significant difference existed between each time interval (control, 7.5, 15, 30, and 60 min, respectively) within a given group (vagotomized and vagally intact). If the absolute values obtained for a physiological variable were not normally distributed, Friedman's repeated measures analysis of variance was employed. If a significant difference existed among time intervals, individual comparisons were made by using the Student-Newman-Keuls post hoc test. Unpaired t-tests or their nonparametric equivalent, the Mann-Whitney U-test, were used to determine whether differences existed between intact and vagotomized cats at selected time intervals. The Bonferroni correction factor for multiple comparisons was applied. All values in the text and figures are presented as means ± SE, and the level of significance chosen was P < 0.05.
RESULTS
Figures 1 and 2 show VT and the iEMG activities
recorded from a vagotomized and vagally intact cat, respectively,
before, during, and after carotid sinus nerve stimulation. Note that
LTF of nasal dilator and genioglossus muscle activities occurs
throughout the poststimulation period in the vagotomized cat (Fig. 1)
and that this response is absent during the poststimulation period in
the vagally intact cat (Fig. 2).
Figure 3 shows the average inspired
VT, and diaphragm, genioglossus,
and nasal dilator muscle iEMG activities that were recorded from the
vagotomized and vagally intact cats under control conditions. Control
conditions were established by setting the end-tidal
CO2 level ~2 Torr above the
threshold for respiratory-related upper airway muscle activities. This
figure demonstrates that the VT and diaphragm activities recorded from both groups were significantly greater than the upper airway muscle activities when all the values were expressed as a percentage of the maximal response to hypercapnia. This occurred because the CO2
level required to activate the upper airway muscles was significantly
greater than the eupneic CO2 level
in these spontaneously breathing cats. Figure 3 also demonstrates that
the VT measured from the
vagotomized animals was greater than the values measured from the
vagally intact animals. The maximum
VT that was measured in response
to hypercapnia at the end of each experiment averaged 127.4 ± 22.6 ml in the vagotomized cats and 95.9 ± 14.5 ml in the vagally intact
cats, respectively.
P < 0.05.
Figure 4 shows the average values for VT and diaphragm, nasal dilator, and genioglossus muscle iEMG activities recorded from the vagotomized and vagally intact cats during the poststimulation period. The VT and iEMG activities were standardized by calculating the difference between the poststimulation values and the control values shown in Fig. 3. Figure 4 demonstrates that the average VT and nasal dilator and genioglossus muscle iEMG activities were significantly greater throughout the poststimulation period in the vagotomized cats, whereas diaphragm activities did not change significantly.
Although similar diaphragm and
VT responses were observed in
the vagally intact cats (Fig. 4), no significant increases in nasal
dilator and genioglossus muscle iEMG activities were recorded during
the poststimulation period. Consequently, nasal dilator and
genioglossus muscle activities recorded during the earlier segments of
the poststimulation period were significantly less than the values
calculated for the vagotomized animals. The magnitude of this
difference diminished during the latter half of the poststimulation period as indicated by the gradual increase in iEMG activities that
were recorded from the vagally intact cats. Figure
5 shows that the changes in
VT and muscle activities
recorded from the vagotomized and vagally intact animals were not
accompanied by significant changes in
TI,
TE, or breathing frequency.
)
and vagally intact cats (
) during prestimulus control conditions and
at various time intervals after 5th stimulation period.
Figure 6 shows that fluctuations in
PaCO2 were minimized throughout the
experimental protocol and poststimulation period. PaCO2 values recorded from the vagally
intact animals tended to be greater than the values recorded from the
vagotomized animals, although this difference was not significant.
PaO2 was maintained at hyperoxic levels
in all experiments (range 217-472 Torr). No significant change in
MAP occurred during the initial 30 min of the poststimulation period.
However, the decrease in MAP at 60 min poststimulation reached
statistical significance in the vagotomized cats. There was no
significant difference in the MAP values recorded from the vagally
intact and vagotomized animals.
) and vagally intact cats () during prestimulus control
conditions and at various time intervals after 5th stimulation period.
Note that PaCO2 did not vary by more
than ±1 Torr during poststimulation period in vagotomized and
vagally intact cats. Significantly different from control,
* P < 0.05.
DISCUSSION
The present investigation showed that LTF of genioglossus and nasal dilator muscle activities can be evoked by carotid sinus nerve stimulation in cerebellum-intact vagotomized cats and that LTF is inhibited in vagally intact cats. The results also show that LTF of inspired VT exceeds that of diaphragm EMG activity, although this latter finding may only pertain to situations when PaCO2 is relatively high.
Critique of methods. The facilitation of VT and EMG activities recorded during the poststimulation period might have been elicited by at least three mechanisms other than the LTF mechanism. First, a decrease in the depth of anesthesia may have evoked the observed responses. However, if this occurred, the activities recorded from the vagotomized animals would have gradually increased throughout the poststimulation period. In contrast, the responses recorded remained constant or decreased throughout this interval. Furthermore, if changes in the depth of anesthesia were responsible for the observed results, similar responses would have been observed in the vagotomized and vagally intact cats. Second, a gradual increase in PaCO2 may have caused the long-lasting facilitatory response recorded during the poststimulation period. However, the changes in PaCO2 were minimized and often did not vary by more than ±1 Torr compared with baseline levels, in both the vagotomized and vagally intact cats. Third, a decrease in MAP could have increased the PCO2 of the extracellular fluid that surrounds the central chemoreceptors despite the maintenance of PaCO2. This probably did not occur in this investigation because MAP was stable in the vagally intact group throughout the poststimulation period. Furthermore, MAP remained stable in the vagotomized group for 30 min poststimulation, and although MAP decreased significantly at 60 min poststimulation it was not accompanied by any significant change in VT or iEMG activities. Given the above arguments, we believe that LTF was responsible for the changes in VT and upper airway muscle activities that were observed after episodic stimulation of a carotid sinus nerve. Nevertheless, it has been suggested that electrical stimulation of carotid sinus nerves may introduce a nonphysiological stimulus to the central nervous system because the fibers that form this nerve rarely fire synchronously at the frequency (25 Hz) employed in this investigation (13). However, previous investigations have shown that repeated episodes of isocapnic hypoxia (which is a more physiologically relevant stimulus than carotid sinus nerve stimulation) can also elicit LTF of phrenic and hypoglossal nerve activities in vagotomized animals (1, 8, 14). Thus our results, which were obtained with electrical stimulation of a carotid sinus nerve, are consistent with data obtained by subjecting animals to isocapnic hypoxia. Carotid sinus nerve stimulation-induced LTF of upper airway and inspiratory muscles in vagotomized cats. A number of investigations have shown that LTF of phrenic and inspiratory intercostal nerve activities can be elicited in vagotomized animals by stimulation of the carotid bodies or carotid sinus nerve (1, 3, 8, 14). In contrast, whether or not episodic carotid sinus nerve stimulation induces LTF in upper airway motoneurons is uncertain. Jiang et al. (10) found no evidence for carotid sinus nerve stimulation-induced LTF of hypoglossal nerve activity in decerebrate/decerebellated cats, whereas Bach and Mitchell (1) observed hypoxia-induced LTF of hypoglossal nerve activity in intact rats. Bach and Mitchell (1) suggested that this difference was not species dependent but was caused by decerebellation of the cats used in the Jiang et al. (10) study. This hypothesis is supported by the results obtained from the present investigation, which showed that LTF of genioglossus and nasal dilator muscle activities can be evoked in the cerebellum-intact, vagotomized, spontaneously breathing cat. Genioglossus and nasal dilator muscle activities increased by 15% compared with baseline values. This increase is similar to values reported for the LTF recorded from inspiratory intercostal nerves, which increased on average 20% above baseline values after episodic carotid sinus nerve stimulation (6). Thus the cerebellum may have a role in the development of LTF in upper airway muscles. The importance of the cerebellum in the development of LTF was demonstrated previously by Hayashi et al. (8), who showed that carotid sinus nerve stimulation-induced LTF cannot be elicited in the phrenic nerve of decerebellated rats. Although LTF was observed in the iEMG activities of the upper airway muscles, no significant facilitation of mean diaphragm muscle activity was recorded in the vagotomized cats. It is possible that the diaphragm muscle activities, which were elevated under control conditions because we increased PaCO2 levels to elicit respiratory-related upper airway muscle activities (see Fig. 3), may have obscured LTF due to saturation of phrenic motoneuronal activity. This suggestion is supported by the findings of Eldridge et al. (4), who showed that phrenic nerve activities can saturate as respiratory drive is increased with hypercapnia. Nevertheless, this explanation does not account for the varying degree of LTF of VT and diaphragm activities because the activities of these two variables were similar under control conditions. The significant LTF of inspired VT, which presumably was generated by the activation of primary and accessory inspiratory muscles, may have occurred because the effect of serotonergic inputs on accessory muscle motoneurons might be greater than the effect on phrenic motoneurons. This suggestion is supported by the findings of Fregosi and Mitchell (6), who showed that LTF of inspiratory intercostal nerve activities was greater than that recorded from the phrenic nerve and that LTF recorded from these two nerves was mediated by a serotonergic mechanism. Similarly, Jiang and Shen (11) found a greater density of serotonergic terminals on inspiratory intercostal motoneurons compared with that on phrenic motoneurons. Carotid sinus nerve stimulation-induced LTF of upper airway and inspiratory muscles in vagally intact cats. We hypothesized that the degree of LTF of inspiratory and upper airway muscle activities observed in vagotomized animals might be reduced in intact animals by a long-lasting inhibitory memory, which could be elicited by repeated stimulation of lung-stretch receptors. This hypothesis was based on the observation that the activities of motor nerves innervating the nasal dilator, genioglossus, and diaphragm muscles are reduced in response to lung inflations (2, 9, 12) and increased when lung inflation is prevented (16, 19). Furthermore, Xi et al. (21) reported that short-term potentiation of ventilation after exposure to hypoxia was significantly greater in dogs after the vagus nerves were cooled. Finally, Bach and Mitchell (1) and Hayashi et al. (8) showed that episodic hypoxic stimulation of the carotid bodies evoked simultaneously a long-term inhibitory memory and LTF of phrenic and hypoglossal nerve activities. In their studies, LTF was attenuated during the early part of the posthypoxic period before gradually increasing as the inhibitory memory diminished. The present investigation also suggests that a long-lasting vagal inhibitory memory can be activated by repeated stimulation of lung-stretch receptors because LTF of upper airway muscle activities in the vagally intact cats was significantly less compared with the responses recorded in the vagotomized cats during the initial portion of the poststimulation period. However, it is of interest that the inhibitory memory did not attenuate VT or diaphragm activities. There are at least two explanations for the observed differences between upper airway and chest wall muscle activities. First, many investigators have suggested that afferent influences from stretch receptors are differentially distributed to motoneurons innervating upper airway muscles and the diaphragm (9, 16, 19). This hypothesis is based on the observation that periodically withholding lung inflation in decerebrate servo-ventilated cats results in a greater augmentation of hypoglossal and facial nerve activities compared with that recorded from the phrenic nerve (9). Second, the effect of the vagal inhibitory memory on diaphragm and especially accessory inspiratory muscle motoneurons may have been overridden by the elevated level of excitation of these motoneuron pools (6). This suggestion is supported primarily by the VT response that was observed in the vagally intact cats during the poststimulation period. VT was significantly greater than control throughout the poststimulation period, in contrast to the response measured from the upper airway muscles. Nevertheless, the pattern of development was similar to that observed for the upper airway muscles, in that LTF of VT gradually increased throughout the poststimulation period. This finding suggests that the inhibitory memory may have been present during the initial portion of the poststimulation period but was overridden by excitatory inputs to the accessory muscle motoneurons. Physiological significance. The physiological significance of LTF of upper airway muscle activities in humans is uncertain. However, Bach and Mitchell (1) suggested recently that this mechanism may be activated in individuals with obstructive sleep apnea. This syndrome is characterized by periodic narrowing of the upper airway during sleep, which may be accompanied by arterial hypoxemia. Thus repeated episodes of hypoxemia could activate the upper airway motoneuron pools via the carotid bodies, the result being an increase in upper airway muscle tone that could contribute to maintenance of upper airway patency. If this hypothesis is correct, then upper airway muscle iEMG activities during sleep should be greater in individuals with obstructive sleep apnea. Support for this hypothesis comes from the findings of Suratt et al. (18), which showed that alae nasi and genioglossus muscle activities during sleep are greater in patients with obstructive sleep apnea than in control subjects. Given the findings of the present investigation, a long-lasting inhibitory vagal memory could also be activated in individuals with obstructive sleep apnea because the termination of most apneic events is accompanied by marked elevations in VT. Repeated elevations of VT could conceivably activate the vagal inhibitory memory. Activating this memory could cause further instability of the upper airway because of a reduction in muscle tone, if this mechanism was more dominant than LTF. However, the vagal inhibitory memory may be less dominant than the LTF mechanism in humans because the relative strength of afferent stretch-receptor input may be less in humans than in other mammals (20).ACKNOWLEDGEMENTS
This study was supported by National Heart, Lung, and Blood Institute Grants HL-41790 and HL-51056 (to R. F. Fregosi). J. H. Mateika was supported by an American Heart Association, Arizona Affiliate, postdoctoral fellowship and Grant AZFW-1-95. J. H. Mateika is presently an assistant professor in the Departments of Biobehavioral Sciences and Rehabilitation Medicine, Teachers College, Columbia University.
FOOTNOTES
Address for reprint requests: R. F. Fregosi; Dept. of Physiology, Gittings Bldg., Univ. of Arizona, Tucson, AZ 85721-0093.
Received 22 May 1996; accepted in final form 27 September 1996.
REFERENCES
| 1. | Bach, K. B., and G. S. Mitchell. Hypoxia induced long term facilitation of respiratory activity is serotonin dependent. Respir. Physiol. 104: 251-260, 1996. [Medline] |
| 2. |
Brouillette, R. T.,
and
B. T. Thach.
Control of genioglossus muscle inspiratory activity.
J. Appl. Physiol.
49:
801-808,
1980.
|
| 3. |
Cao, K. Y.,
C. W. Zwillich,
M. Berthon-Jones,
and
C. E. Sullivan.
Increased normoxic ventilation induced by repetitive hypoxia in conscious dogs.
J. Appl. Physiol.
73:
2083-2088,
1992.
|
| 4. |
Eldridge, F.,
L. Gill-Kumar,
and
D. E. Millhorn.
Input-output relationships of central neural circuits involved in respiration in cats.
J. Physiol. Lond.
311:
81-95,
1981.
|
| 5. | Fregosi, R. F. Changes in the neural drive to abdominal expiratory muscles in hemorrhagic hypotension. Am. J. Physiol. 266 (Heart Circ. Physiol.) 35: H2423-H2429, 1994. |
| 6. |
Fregosi, R. F.,
and
G. S. Mitchell.
Long term facilitation of inspiratory intercostal nerve activity following carotid sinus nerve stimulation in cats.
J. Physiol. Lond.
477:
469-479,
1994.
|
| 7. | Gesell, R., and M. A. Hamilton. Reflexogenic components of breathing. Am. J. Physiol. 133: 694-719, 1941. |
| 8. |
Hayashi, F.,
S. K. Coles,
K. B. Bach,
G. S. Mitchell,
and
D. R. McCrimmon.
Time-dependent phrenic nerve responses to carotid afferent activation: intact vs. decerebellate rats.
Am. J. Physiol.
265 (Regulatory Integrative Comp. Physiol. 34):
R811-R819,
1993.
|
| 9. | Hwang, J. C., C. T. Chien, and W. M. St. John. Characterization of respiratory-related activity of the facial nerve. Respir. Physiol. 73: 175-188, 1988. [Medline] |
| 10. | Jiang, C., G. S. Mitchell, and J. Lipski. Prolonged augmentation of respiratory discharge in hypoglossal motoneurons following superior laryngeal nerve stimulation. Brain Res. 538: 215-225, 1991. [Medline] |
| 11. | Jiang, Z.-H., and E. Shen. Synaptic connection between monoaminergic terminals and intercostal respiratory motoneurones in cats. Acta Physiol. Sin. 37: 479-485, 1985. |
| 12. |
Kuna, S. T.
Inhibition of inspiratory upper airway motoneuron activity by phasic volume feedback.
J. Appl. Physiol.
60:
1373-1379,
1986.
|
| 13. | Lahiri, S., and R. G. DeLaney. Stimulus interaction in the responses of carotid body chemoreceptor single afferent fibers. Respir. Physiol. 24: 249-266, 1975. [Medline] |
| 14. | Millhorn, D. E., F. L. Eldridge, and T. G. Waldrop. Prolonged stimulation of respiration by a new central neural mechanism. Respir. Physiol. 41: 87-103, 1980. [Medline] |
| 15. | Millhorn, D. E., F. L. Eldridge, and T. G. Waldrop. Prolonged stimulation of respiration by endogenous central serotonin. Respir. Physiol. 42: 171-188, 1980. [Medline] |
| 16. |
Strohl, K. P.
Respiratory activation of the facial nerve and alar muscles in anaesthetized dogs.
J. Physiol. Lond.
363:
351-362,
1985.
|
| 17. |
Strohl, K. P.,
C. E. O'Cain,
and
A. S. Slutsky.
Alae nasi activation and nasal resistance in healthy subjects.
J. Appl. Physiol.
52:
1432-1437,
1982.
|
| 18. | Suratt, P., R. F. McTier, and S. C. Wilhoit. Upper airway muscle activation is augmented in patients with obstructive sleep apnea compared with that in normal subjects. Am. Rev. Respir. Dis. 137: 889-894, 1988. [Medline] |
| 19. |
Van Lunteren, E.,
K. P. Strohl,
D. M. Parker,
E. N. Bruce,
and
W. B. Van De Graaff.
Phasic volume-related feedback on upper airway muscle activity.
J. Appl. Physiol.
56:
730-736,
1984.
|
| 20. | Widdicombe, J. G. Respiratory reflexes in man and other mammalian species. Clin. Sci. Lond. 21: 163-170, 1961. [Medline] |
| 21. |
Xi, L.,
C. A. Smith,
K. W. Saupe,
and
J. A. Dempsey.
Effects of memory from vagal feedback on short-term potentiation of ventilation in conscious dogs.
J. Physiol. Lond.
462:
547-561,
1993.
|
This article has been cited by other articles:
|
|
 |
|
  K.-Z. Lee, P. J. Reier, and D. D. Fuller Phrenic Motoneuron Discharge Patterns During Hypoxia-Induced Short-Term Potentiation in Rats J Neurophysiol, October 1, 2009; 102(4): 2184 - 2193. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Ryan and P. Nolan Long-term facilitation of upper airway muscle activity induced by episodic upper airway negative pressure and hypoxia in spontaneously breathing anaesthetized rats J. Physiol., July 1, 2009; 587(13): 3343 - 3353. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Ryan and P. Nolan Episodic hypoxia induces long-term facilitation of upper airway muscle activity in spontaneously breathing anaesthetized rats J. Physiol., July 1, 2009; 587(13): 3329 - 3342. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. H. Mateika and G. Narwani Intermittent hypoxia and respiratory plasticity in humans and other animals: does exposure to intermittent hypoxia promote or mitigate sleep apnoea? Exp Physiol, March 1, 2009; 94(3): 279 - 296. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. McGuire, C. Liu, Y. Cao, and L. Ling Formation and maintenance of ventilatory long-term facilitation require NMDA but not non-NMDA receptors in awake rats J Appl Physiol, September 1, 2008; 105(3): 942 - 950. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Wadhwa, C. Gradinaru, G. J. Gates, M. S. Badr, and J. H. Mateika Impact of intermittent hypoxia on long-term facilitation of minute ventilation and heart rate variability in men and women: do sex differences exist? J Appl Physiol, June 1, 2008; 104(6): 1625 - 1633. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Rowley, I. Deebajah, S. Parikh, A. Najar, R. Saha, and M. S. Badr The influence of episodic hypoxia on upper airway collapsibility in subjects with obstructive sleep apnea J Appl Physiol, September 1, 2007; 103(3): 911 - 916. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. P. Harris, A. Balasubramaniam, M. S. Badr, and J. H. Mateika Long-term facilitation of ventilation and genioglossus muscle activity is evident in the presence of elevated levels of carbon dioxide in awake humans Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2006; 291(4): R1111 - R1119. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. John, E. F. Bailey, and R. F. Fregosi Respiratory-related Discharge of Genioglossus Muscle Motor Units Am. J. Respir. Crit. Care Med., November 15, 2005; 172(10): 1331 - 1337. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. McGuire, Y. Zhang, D. P. White, and L. Ling Phrenic long-term facilitation requires NMDA receptors in the phrenic motonucleus in rats J. Physiol., September 1, 2005; 567(2): 599 - 611. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. D. Fuller Episodic hypoxia induces long-term facilitation of neural drive to tongue protrudor and retractor muscles J Appl Physiol, May 1, 2005; 98(5): 1761 - 1767. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. C. McKay, W. A. Janczewski, and J. L. Feldman Episodic hypoxia evokes long-term facilitation of genioglossus muscle activity in neonatal rats J. Physiol., May 15, 2004; 557(1): 13 - 18. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Babcock, M. Shkoukani, S. E. Aboubakr, and M. S. Badr Determinants of long-term facilitation in humans during NREM sleep J Appl Physiol, January 1, 2003; 94(1): 53 - 59. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C.-s. Yan, Y. K. Vohra, H.-k. Mao, and R. J. Hemley Very high growth rate chemical vapor deposition of single-crystal diamond. PNAS, October 1, 2002; 99(20): 12523 - 12525. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Shkoukani, M. A. Babcock, and M. S. Badr Effect of episodic hypoxia on upper airway mechanics in humans during NREM sleep J Appl Physiol, June 1, 2002; 92(6): 2565 - 2570. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. E. Aboubakr, A. Taylor, R. Ford, S. Siddiqi, and M. S. Badr Long-term facilitation in obstructive sleep apnea patients during NREM sleep J Appl Physiol, December 1, 2001; 91(6): 2751 - 2757. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. B. Olson Jr., C. J. Bohne, M. R. Dwinell, A. Podolsky, E. H. Vidruk, D. D. Fuller, F. L. Powell, and G. S. Mitchel Ventilatory long-term facilitation in unanesthetized rats J Appl Physiol, August 1, 2001; 91(2): 709 - 716. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. S. Mitchell, T. L. Baker, S. A. Nanda, D. D. Fuller, A. G. Zabka, B. A. Hodgeman, R. W. Bavis, K. J. Mack, and E. B. Olson Jr. Physiological and Genomic Consequences of Intermittent Hypoxia: Invited Review: Intermittent hypoxia and respiratory plasticity J Appl Physiol, June 1, 2001; 90(6): 2466 - 2475. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. Janssen and R. F. Fregosi No evidence for long-term facilitation after episodic hypoxia in spontaneously breathing, anesthetized rats J Appl Physiol, October 1, 2000; 89(4): 1345 - 1351. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. L. Janssen, J. S. Williams, and R. F. Fregosi Consequences of periodic augmented breaths on tongue muscle activities in hypoxic rats J Appl Physiol, May 1, 2000; 88(5): 1915 - 1923. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. MATEIKA, D. L. MILLROOD, J. KIM, H. P. RODRIGUEZ, and G. J. SAMARA Response of Human Tongue Protrudor and Retractors to Hypoxia and Hypercapnia Am. J. Respir. Crit. Care Med., December 1, 1999; 160(6): 1976 - 1982. [Abstract] [Full Text]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
