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Department of Applied Physiology, Ruhr-University Bochum, D-44780 Bochum, Germany
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Rapid eye
movements during rapid-eye-movement (REM) sleep are associated with
rapid, shallow breathing. We wanted to know whether this
effect persisted during increased respiratory drive by
CO2. In eight healthy subjects, we
recorded electroencephalographic, electrooculographic, and
electromyographic signals, ventilation, and end-tidal
PCO2 during the night. Inspiratory
PCO2 was changed to increase
end-tidal PCO2 by 3 and 6 Torr. During normocapnia, rapid eye movements were associated with a decrease
in total breath time by 
0.71 ± 0.19 (SE) s
(P < 0.05) because of shortened
expiratory time (0.52 ± 0.08 s,
P < 0.001) and with a reduced tidal
volume (89 ± 27 ml, P < 0.05) because of decreased rib cage contribution (75 ± 18 ml, P < 0.05). Abdominal (11 ± 16 ml, P = 0.52) and minute
ventilation (0.09 ± 0.21 ml/min, P = 0.66) did not change. In
hypercapnia, however, rapid eye movements were associated with a
further shortening of total breath time. Abdominal breathing was also
inhibited (79 ± 23 ml, P < 0.05), leading to a stronger inhibition of tidal volume and minute
ventilation (1.84 ± 0.54 l/min,
P < 0.05). We conclude that
REM-associated respiratory changes are even more pronounced during
hypercapnia because of additional inhibition of abdominal breathing.
This may contribute to the reduction of the hypercapnic ventilatory response during REM sleep.
compartmental ventilation; control of breathing; rib cage; abdomen
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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IRREGULAR BREATHING IS A COMMON feature of rapid-eye-movement (REM) sleep. Since the original description of REM sleep by Aserinsky and Kleitman (3) in 1953, several studies have investigated the correlation of phasic eye movements and changes in respiratory patterns (1, 2, 4, 6, 9, 15, 16). Quantitative analyses by Millman et al. (15) and Gould et al. (9) showed that increasing eye-movement activity was associated with a reduction in tidal volume (VT) and a shortening of total breath time (TT), whereas inspiratory time (TI) was unchanged. This association of phasic events and changes in respiration causing the irregularity remained unchanged in the course of the night, although the frequency of events increased from early to late REM sleep (16).
We wanted to know whether these inhibitory effects on VT and the offsetting increase in respiratory rate were attenuated by hypercapnia during stimulated breathing, or whether they persisted and could contribute to an explanation for the diminished hypercapnic ventilatory response during REM sleep compared with wakefulness as described by Phillipson et al. (21) in the dog and Douglas et al. (7) in humans. We have, therefore, tested the effect of different levels of hypercapnia on the ventilatory pattern in the presence vs. absence of rapid eye movements during REM sleep in healthy subjects.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Subjects
The study was performed in eight healthy men, who ranged in age from 24 to 32 yr. They were nonobese without a history of cardiac, pulmonary, neurological, or sleep-related breathing disorders. No subject was taking psychotropic drugs or other regular medications. Each participating subject gave informed and written consent. The study was approved by the ethics committee of the Faculty of Medicine at the Ruhr-University Bochum.Protocol
Subjects reported to the sleep laboratory at 9 PM. Before formally entering the study, each subject underwent lung function testing and a general examination. Then they were prepared for polysomnography. Electrodes were attached to the scalp by using the international 10/20 system, to the skin 1 cm lateral and 1 cm above (right) and below (left) the canthi, and to the submental regions according to Rechtschaffen and Kales (22). Thus two electroencephalographic (EEG) signals (C3-A2, C4-A1), a bipolar electrooculographic (EOG) signal, and a bipolar electromyographic (EMG) signal were continuously recorded on a polygraph (Schwarzer-Picker ED14 Digital). The EEGs and the EOG were filtered with time constants of 0.3 s (high-pass) and a low-pass filter of 30 Hz.Ventilation was measured by pneumotachography (PT; ScreenMate, Jaeger, Würzburg, Germany) by using a comfortably fitting nose mask (nasal continuous positive airway pressure mask; Respironics) and was measured noninvasively by means of respiratory inductive plethysmography (RIP; Respitrace, Ambulatory Monitoring, Ardsley, NY). Inductive bands were secured with adhesive tape around the chest and abdomen. To obtain the calibration factors for the inductive plethysmograph, the subjects performed isovolume maneuvers (14) in the supine position, during which gains of the rib cage (RC) and abdominal (Abd) channels were adjusted, until the resulting sum of the two signals (Sum) was zero. Afterwards, the three RIP signals (RC and Abd motion and Sum) were recorded, together with the PT signal, by using a mouthpiece and nose clip during 3 min of the subjects' breathing with different VT and compartmental volume to validate the RIP calibration. The correlation of RIP and PT was calculated by least squares linear regression. The regression coefficients were highly significant [r = 0.96 ± 0.02 (SD), P < 0.001] in all eight subjects.
The RIP and the PT signal flow and volume were recorded simultaneously on a chart recorder together with the EEG data and end-tidal PCO2 (PETCO2) and PO2 by means of an infrared CO2 and paramagnetic O2 analyzer (Normocap 200 Oxy, Datex, Helsinki, Finland). The PT was then attached to the outlet of a constant stream of gas flow (60 l/min) supplied by an air pump. The PT was calibrated by injection of 1 liter of air into the circuit at the constant background flow. The subject's nose mask was then attached to the circuit so that he could breathe from and into the background flow. This setup enabled easy changes of the inspired-gas composition without the need of valves. All data were fed into an analog-digital converter (CED 1401 plus, Cambridge Electronic Design, Cambridge, UK) and stored on hard disk. During the entire night's sleep, the measurements were monitored on the paper polygraph and the personal computer screen.
To get different steps of inspiratory and thus alveolar and arterial PCO2 during REM sleep, CO2 was added to the inspiratory line so that the PETCO2 was increased by 3 and 6 Torr, respectively, every 6-7 min. Thus one cycle with baseline PETCO2, increased by 3 and 6 Torr, lasted 20 min.
Data Processing
At first the paper records were scored, according to the rules of Rechtschaffen and Kales (22), by two independent observers to identify clear REM sleep periods. Ventilation during these REM periods was analyzed breath by breath by using a computer-based analysis system developed in our laboratory on the basis of the Spike2 laboratory software package (CED). For each breath, the PT and the three RIP signals, RC, Abd, and Sum, as well as gas concentrations of O2 and CO2 in the inspired and expired air, were displayed consecutively on the screen, together with markers indicating the detected TI and expiratory times (TE) and amplitudes to check the computerized analysis. The program provided tabular listings of the following variables: 1) respiratory timing: described by TT, TI, TE, and respiratory duty cycle (TI/TT); and 2) VT: VT calculated by digital integration of the airflow signal obtained from the PT (VTPT), rib cage (VTrc), and abdominal (VTabd) compartmental volumes from the RIP signal, as well as PETCO2. The simultaneous EOG segments were analyzed by means of a fast Fourier transformation. The resulting total power density was a highly sensitive parameter to identify rapid eye movements. In parallel, a visual analysis of eye movements was performed by application of scoring criteria adapted from Neilly et al. (16) for bipolar recordings. By comparison with the visually obtained data, a threshold in total power density for detection of rapid eye movements was defined for each subject. Each set of data was carefully checked. A total of 75 ± 27 s (range 0-191 s) was excluded from the analysis because of artifacts, EEG arousals (increased mean EEG frequency > 16 Hz lasting 3-30 s and increases in chin EMG), and/or movement artifacts in respiratory signals.Analysis of PETCO2
Because of intermittent small breaths, end-tidal plateaus were not always achieved for each breath. Only breaths with a true end-tidal plateau were included in the calculation of the step changes in PETCO2. Overall, 8.4 ± 0.5 (SD) % of breaths were excluded from the analysis of the PETCO2.Validation of VT Measurements
Stability of the PT signal. After calibration of the PT in the evening by means of a 1,000-ml calibration syringe, application of the same volume after ~7 h in the morning resulted in a reading of 995 ± 17 ml (range 981-1,021 ml). The differences from the initial calibration values were not significant (P > 0.47, paired t-test).
Detection of mouth breathing. The subject's mouth was not taped shut for safety reasons and to minimize disturbances. Mouth opening was detected by means of the PT by a drop or rise of the ratio of separately measured inspiratory to expiratory volumes, in conjunction with a decrease of the ratio of VTPT to the VT estimates of the RIP (VTRIP), provided that there were no movement-related changes in the RIP signal. Overall, a 10-min episode of mouth breathing in one subject was excluded from the analysis.
Validation of RIP data. Although the RIP method has been shown to give a good estimate of VT after appropriate calibration (5), there is considerable doubt over its accuracy during a whole night's sleep after only one initial calibration procedure (27). In our study, we profited by the fact that VT were simultaneously measured by means of the PT and the RIP. In addition to the initial calibration procedure, the VTRIP were correlated with the VTPT for each REM sleep episode. The mean of the correlation coefficients between VTPT and VTRIP was 0.97 ± 0.02 (SD). VT, respiratory timing, and ventilation were calculated by using the PT signal. Compartmental ventilation (VTrc and VTabd) was analyzed by using the RIP signal. For breaths to be accepted, the difference between VTPT and VTRIP had to be <10%. This was the case in 3,625 of 4,455 breaths (81.4%).
Timing Between Rapid Eye Movements and Breaths
As the density and the timing of eye movements have an effect on the magnitude of changes in ventilation (9, 15), we further restricted the analysis to those breaths that occurred during a burst of eye movements, with the preceding and following breaths also associated with eye-movement activity designated as REM+. These breaths were compared with breaths called REM, which occurred within a REM
sleep period but were not associated with any eye movement. There was
at least one breath interspersed between REM breaths and
preceding or following eye-movement activity. A total number of 1,994 breaths (44.8%) fulfilled these criteria and was included in the analysis.
Statistical Methods
From the tables containing the breath-by-breath information, we calculated mean values of breaths in the absence of rapid eye movements (REM) and the means of those coinciding with rapid eye movements
(REM+) for each of the three CO2
steps in the eight subjects. The data were entered into an ANOVA by
CO2 step (0, 1, or 2) and by REM
activity (0 or 1) with a repeated-measurement design by using SPSS V.6.
If significant differences were shown to exist between the group means,
comparisons were made by using paired
t-tests. The level of significance was
corrected by using the Bonferroni method. A
P value < 0.05 was considered
significant. Data are expressed as means ± SE unless otherwise stated.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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REM sleep was recorded in all eight subjects. Eighteen REM sleep
periods (mean duration 19.6 ± 2.9 min, total duration 353 min) were
included in the analysis. From a total of 1,994 breaths that met the
inclusion criteria, 1,397 (70.1%) occurred in the absence of rapid eye
movements (REM) and 597 (29.9%) in the presence of rapid eye
movements (REM+). With respect to
CO2 steps, 494 breaths occurred
during normocapnia, 828 during the first step of hypercapnia, and 672 during the second. The baseline
PETCO2 of 40.9 ± 1.0 Torr was increased to 44.1 ± 0.8 Torr in the first step of
hypercapnia and to 46.8 ± 0.7 Torr in the second step by adding
CO2 to the inspired air. Figure
1 shows an original recording including a
step change in the inspiratory CO2
partial pressure.
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Differences between mean values obtained from breaths in the absence and presence of rapid eye movements are shown in Fig. 2. During normocapnia, breaths coinciding with rapid eye movements had a smaller VT (405 ± 29 ml), compared with breaths in the absence of rapid eye movements (495 ± 26 ml, P < 0.05), due to an inhibition of rib cage movements (120 ± 19 vs. 195 ± 23 ml, P < 0.05). The TT was shorter (3.6 ± 0.2 vs. 4.3 ± 0.1 s, P < 0.05) because of a shorter TE, i.e., respiratory rate increased from 14.0 to 16.8 breaths/min during rapid eye movements. These effects, however, were offsetting. Minute ventilation [6.86 ± 0.48 vs. 6.96 ± 0.39 l/min, not significant (NS)] remained unchanged during rapid eye movements.
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Increasing hypercapnia during REM sleep led to an overall increase of
VT and rib cage and abdominal
breathing movements and a shortening of
TT,
TI, and
TE, resulting in an increased
minute ventilation (Fig. 2). Under these hypercapnic conditions,
breaths in the presence of rapid eye movements, compared with those
without rapid eye movements, showed differences in the same directions as observed during normocapnia but were even more pronounced (see Fig.
3 for details of proportional changes
during rapid eye movements compared with in the absence of rapid eye
movements). In addition, abdominal breathing movements were now reduced
during rapid eye movements by 24 ± 15 ml (NS) in the first
CO2 step and by 79 ± 23 ml
(P < 0.05) in the second. These
differences also affected ventilation, as minute ventilation was also
smaller during rapid eye movements (0.61 ± 0.44 l/min, NS,
first step of hypercapnia; and 1.84 ± 0.54 l/min,
P < 0.05, second step) in
hypercapnia (Figs. 2 and 3).
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Hypercapnia had a significant modulating influence on REM-associated changes of respiratory patterns. The ANOVA revealed a significant influence of the end-expiratory CO2 level on differences in abdominal contribution and minute ventilation, which were more and more reduced in the presence of rapid eye movements, compared with in the absence of rapid eye movements, with higher levels of hypercapnia (P < 0.05, Fig. 3). Changes in all other measures, TT, TI, and TE, duty cycle, and rib cage contribution, were not significantly different among the three CO2 steps.
Subjects with only minor differences in mean respiratory measures between breaths, with and without rapid eye movements, so-called low responders (16), were hard to find. At least during increased respiratory drive, relative differences in respiratory timing or VT exceeded reductions of 10% from baseline values. Figure 4 demonstrates that there was a strong correlation between the reduction in VT and the increase in respiratory frequency, with a tendency to stabilize minute ventilation by offsetting effects. Within-subject differences and the tendency to stronger effects during hypercapnia (see Fig. 3) can be seen.
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The present study demonstrates that phasic REM activity coincides with typical changes of respiratory measures even under the conditions of increased respiratory drive by hypercapnia. Our results extend previous findings of interactions during normocapnia (2, 4, 15, 16) and hypercapnia (25), presenting quantitative data on REM-associated changes in respiratory timing, VT, compartmental volume, and ventilation in relation to increased chemical drive of respiration. One observation of interest is that respiratory changes during normocapnia are offsetting with respect to ventilation, whereas, with increasing hypercapnia, abdominal breathing movements are more and more inhibited during phasic REM events. This leads to decrements in ventilation, which might be responsible for the observation of attenuated hypercapnic ventilatory responses, as described to occur during phasic REM sleep in dogs (25), or eye-movement-dense REM sleep in humans.
Normocapnia
The results with respect to normocapnia are similar to those reported previously (2, 9, 15). We found eye-movement-related shortening of TT and TE but only small effects on TI. Results on changes in VT and compartmental volume during normocapnia are consistent with the results of previous investigations (15, 16) showing that decrements in the rib cage compartmental ventilation were responsible for the reduced VT during eye-movement activity. When the mean values of minute ventilation that were calculated for breaths in the presence of rapid eye movements were compared with those of breaths without eye movements, there was no significant difference due to offsetting effects of reduced VT and increased respiratory rates. This finding confirms earlier studies performed in infants (10), in which falls in VT and TT were associated with eye-movement activity. Although in that study, instantaneous ventilation did not change, other studies indicated that ventilation was reduced (9, 15). Gould et al. (9) found an 8.7% reduction in minute ventilation in intervals with eye movements compared with those without eye movements. These differences might be due to the mode of analysis used on the background of the large variation of ventilation during REM sleep. Whereas Gould et al. (9) used 20-s epochs with and without eye movements, our results were obtained from pooled data of single breaths with and without eye movements distributed over the REM sleep periods.Hypercapnia
In several studies, phasic irregularities in REM sleep breathing were observed during experimentally increased levels of afferent input to medullary respiratory neurons by hypercapnia. Irregular breathing persisted in the cat (19) and the dog (21, 25) despite progressive hypercapnia. We now can show that, during hypercapnia in men, REM activity affected respiratory timing and rib cage compartmental breathing in a similar manner compared with normocapnia. Relative changes in TT and VTRC of breaths with and without eye movements were not significantly different for the three CO2 levels. Abdominal movements, however, which remained unchanged during normocapnia, showed increasing inhibition with increased levels of respiratory drive. In contrast to normocapnic conditions, ventilation significantly decreased during eye-movement activity in hypercapnia.High and Low Responders
On the basis of the findings of large between-subject differences in respiratory changes during REM sleep, Neilly et al. (16) defined high and low responders to phasic REM events. With respect to these individual characteristics, we observed differential changes in decrements in VT and compartmental volume and increments in respiratory frequency in association with the level of the PCO2. Some individuals had only minor changes, e.g., during normocapnia, but stronger effects during hypercapnia.Mechanisms
Our results could be explained by rapidly increased upper or lower airway resistance coinciding with rapid eye movements during REM sleep. Our data, however, give no information about the behavior of the airway resistance. By means of genioglossus and alae nasi EMGs, Wiegand et al. (28) showed reduced upper airway dilator muscle activation during phasic REM events. Supraglottic pharyngeal resistance, however, did not change significantly during rapid eye movements in normocapnia. On the other hand, there is experimental evidence for centrally mediated effects on respiration during phasic REM activity. Generally, human intercostal EMG activity declines during REM sleep, compared with NREM sleep and wakefulness, whereas diaphragmatic EMG increases (26). Several other studies (15, 16) on the association of phasic REM events with changes in ventilation under normocapnic conditions showed additional inhibition of rib cage motion, whereas very little of the variation in abdominal motion was associated with phasic eye movements. These differences in effects on compartmental ventilation have been related to differences in the response to lesions of brain stem regions that mediate motor atonia during REM sleep. Hendricks et al. (12) showed that elimination of an area in the dorsal pontine tegmentum abolished REM sleep atonia and disinhibited diaphragmatic EMG during inspiratory bursts by increasing the average rate of rise of diaphragmatic activity. Stimulation of this area inhibited phrenic nerve activity only slightly but inhibited intercostal nerves more (13). Thus intrinsic neuronal REM sleep mechanisms seem to trigger both the phasic REM events and the effects on respiration, as suggested by the strong association of pontogeniculooccipital waves with changes in the activity of medullary respiratory neurons (17). These general effects, however, do not explain the CO2-dependent differential effect of eye-movement activity on abdominal breathing and ventilation. Recent studies by Smith et al. (23) on the neural-mechanical coupling of breathing in REM sleep in chronically instrumented dogs may offer an explanation of mechanisms involved. They analyzed the diaphragmatic EMG during airway occlusion in phasic REM sleep, compared with NREM sleep, and found a reduced and more variable diaphragmatic EMG activity during occluded breaths in phasic REM sleep, attributed to a reduced respiratory neural output. Brief interruptions, so-called fractionations (18) of the diaphragm EMG ramp, accounted for at least some of the blunted response to airway occlusion and the related asphyxic blood-gas changes. These fractionations were present in 41% of occluded breaths. In addition, Hendricks and Kline (11) showed considerable regional heterogeneity of fractionations in the costal diaphragm of cats. Thus many local interruptions may occur in different regions of the diaphragm at the same time within one breath, which would impair the recruitment of the diaphragm during increased respiratory drive. Several other mechanisms might also be involved, such as direct interactions of phasic REM events at the level of respiratory neurons, leading to premature switch off of inspiration (23) or interference of phasic events with the central chemosensitive mechanism, either directly or at the level of integration of chemosensory inputs to the neural respiratory network. Even short-term changes in local cerebral blood flow in the central chemosensitive area could account for reductions in ventilation (20). Conclusions about the roles of these mechanisms in the genesis of REM-related changes in diaphragmatic activity are, however, beyond the scope of this paper.Implications
The CO2-dependent differential effect on abdominal breathing might be responsible for the findings of attenuated hypercapnic ventilatory responses during REM sleep (7), despite similar normocapnic ventilation during REM and non-REM sleep (26). The blunted ventilatory response to hypercapnia during eye-movement-dense REM sleep in humans could also account for the prolongation of obstructive apneas observed during REM sleep (24), as during the buildup of asphyxia the ventilatory effort is reduced compared with during NREM sleep. This in turn leads to reduced sensory input from the chest wall, which plays an important role in the occurrence of arousal from sleep and termination of apneas (8).In conclusion, the typical changes in respiration associated with rapid eye movements, e.g., rapid, shallow breathing with predominant effects on rib cage excursions and TE, are by no means attenuated during increased respiratory drive during hypercapnia but are even more pronounced. In addition, abdominal excursions are inhibited, which leads to a decrease in minute ventilation during rapid eye movements with increasing levels of PETCO2.
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ACKNOWLEDGEMENTS |
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The authors thank Sharon W. Garrison for English revision.
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FOOTNOTES |
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Address for reprint requests: T. Schäfer, Ruhr-Universität Bochum, Abt. für angewandte Physiologie, Universitätsstraße 150, D-44780 Bochum, Germany (E-mail: Thorsten.Schaefer{at}ruhr-uni-bochum.de).
Received 30 January 1997; accepted in final form 27 August 1998.
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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 A. K. Curran, R. A. Darnall, J. J. Filiano, A. Li, and E. E. Nattie Muscimol dialysis in the rostral ventral medulla reduced the CO2 response in awake and sleeping piglets J Appl Physiol, March 1, 2001; 90(3): 971 - 980. [Abstract] [Full Text] [PDF]
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E),
VTrc,
VTabd, and
inspiratory time (TI) during
normocapnia (open circles,
PETCO2 = 40.9 Torr), mild
hypercapnia (shaded circles,
PETCO2 = 44.1 Torr), and
stronger hypercapnia (solid circles,
PETCO2 = 46.8 Torr). Values
are means ± SE of 8 subjects. Differences between breaths with and
without eye-movement activity:
* P < 0.05, *** P < 0.001 (ANOVA with
repeated-measurement design);
+ P < 0.05, ++ P < 0.01 (post hoc t-tests with
Bonferroni correction). n.s., Not significant.
) in VT and
TT of breaths in presence
compared with in absence of rapid eye movements tend to offset each
other. 
, Relative changes of
VT and
TT; lines connect data of
individual subjects; arrows at end of lines indicate "hypercapnic
direction"; dotted line, linear regression with corresponding
correlation coefficient r.