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Departments of 1 Pediatrics and 2 Physiology, Medical College of Wisconsin and Zablocki Veterans Affairs Medical Center, Milwaukee 53226; and 3 Department of Physical Therapy, Marquette University, Milwaukee, Wisconsin 53201
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Our aim was to determine the frequency and characteristics of a fractionated pattern of diaphragm and upper airway muscle activity and airflow during wakefulness and sleep in adult goats. A fractionated breath (FBr) was defined as three or more brief (40-150 ms) interruptions in the diaphragm activity not associated with multiple swallows, eructation, mastication, or movement. During a FBr, the discharge pattern in the diaphragm and upper airway muscles showed complete cycles of inspiration and expiration. Whereas the interval between peak diaphragm activity of the breath preceding the FBr to the first diaphragm peak of the FBr was 15-20% less than the average interval of the preceding five control breaths, the breath-to-breath interval of the five breaths after a FBr did not differ from the control breaths before the FBr event. In normal goats, FBr was evident in only 4 of 18 (22%) awake goats and in only one of these goats during non-rapid eye movement sleep. In 35 goats with implanted microtubules in the medulla, FBr were present in 14 (40%) goats. In these goats with FBr, 78% (11 of 14) had one or more implantations into or near the facial, vestibular, or raphe nuclei. The effect of perturbations in these nuclei is probably nonspecific, because injections into these nuclei with mock cerebrospinal fluid or excitatory amino acid-receptor agonist or antagonist produced both increases and decreases in the frequency of the FBr while not altering their characteristics. Finally, a swallow occurred at the termination or during the first breath after 60% of the FBr. We speculate that the FBr manifest 1) the disruption of a neuronal network, which coordinates breathing and other functions (such as swallowing), utilizing the same anatomic structures, and/or 2) transient changes in synaptic inputs that increase the rate of the normal respiratory rhythm generator or allow an ectopic, anomalous generator to become dominant.
respiration; diaphragm; fractionations; pharyngeal muscles; excitatory amino acid receptors
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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REGULAR RHYTHMIC ELECTRICAL activity of the phrenic nerve and diaphragm signifies the oscillatory pattern of the respiratory rhythm generator during physiological conditions (3). Except for a few circumstances that produce within-breath interruptions, this rhythmic activity increases and decreases with increases or decreases in metabolic rate throughout wakefulness and sleep. Within-breath interruptions are associated with the integration of other pattern generators (swallowing, vomiting, regurgitation, etc.) that alter the respiratory rhythm (15). Therefore, of interest was the description of Orem et al. (19, 20) of fractionated diaphragm activity that was associated with active rapid eye movement (REM) sleep. Fractionated breathing (FBr) was characterized by brief interruptions (20-100 ms) in diaphragm muscle activity that were thought to be a result of phasic inhibition of the phrenic motoneurons associated with the occurrence of pontogeniculooccipital (PGO) waves during REM sleep (14, 15, 19, 20). In subsequent studies by Hunt et al. (15), FBr were elicited by auditory tone in all states in freely behaving cats. Similarly, FBr have been observed with an alerting response (acoustic startle reflex) (14) and sniff and aspiration reflex behaviors (1, 6, 25, 26).
While investigating in goats the medullary control of breathing, we observed changes in airflow and diaphragm activity suggesting FBr. The FBr were similar in pattern to that described previously in cats (15, 19, 20), but, in contrast, we observed FBr during wakefulness and non-REM sleep. In addition, these FBr were not associated with eructation, mastication, or multiple swallows. Therefore, we retrospectively investigated the frequency and characteristics of fractionated activity in the diaphragm and upper airway muscles and airflow during wakefulness and sleep in goats. To gain insight into the mechanism of the FBr, we determined the effect of implanting microtubules (MTs) into rostral medullary nuclei and the subsequent injection of mock cerebrospinal fluid (mCSF) or excitatory amino acid (EAA)-receptor agonist and antagonist into these nuclei. Because these injections alter the coordination of breathing and swallowing (8), we also determined the incidence of swallows at the termination and the first breath after a FBr. Finally, because increasing inspired CO2 (hypercapnia) reduces or eliminates many types of periodic or irregular breathing (2, 13, 17), we investigated whether hypercapnia during wakefulness altered FBr.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals. The data from 47 adult goats of various breeds were examined. All goats received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" formulated by the National Research Council in 1996. The Institutional Animal Care Committee of the Medical College of Wisconsin approved the study protocol.
Surgical preparation. All surgeries were performed under sterile conditions. An initial surgery was performed to elevate the carotid arteries and to implant EEG, electrooculographic (EOG), and electromyographic (EMG) electrodes in the diaphragm (EMGDia) and in laryngeal and pharyngeal upper airway muscles. In addition, during the initial surgery in six goats, the upper airway was isolated by creating a tracheostoma at the level of the eighth tracheal ring. A second surgery was performed approximately 4 wk later to implant MTs bilaterally into rostral medullary nuclei. As stated elsewhere (8, 27), we initially targeted the retrotrapezoid nucleus, but the placement was not precise. Thus MTs were also implanted into several other medullary nuclei. Implants were usually placed bilaterally to increase the amount of data obtained from each goat. Anesthesia was induced with an intravenous injection of ketamine (Ketaset) and xylazine (12:1 vol/vol ratio, 15 mg/kg). After intubation for mechanical ventilation, anesthesia was maintained with 1.5% halothane in oxygen (sufficient to eliminate the withdrawal reflex and any signs of pain). Both EMG electrode placement (7-9) and MT implantation have been described previously (27).
To minimize brain edema after implantation surgery, the goats were medicated three times per day with dexamethasone (0.4 mg · kg
1 · day1
for 2 days, then decreasing by 0.05 mg · kg1 · day1).
To minimize infection, chlorampehicol (20 mg/kg) was administered three
times per day for 3 days. Thereafter, the goats received daily
intramuscular injections of antibiotics (ceftiofur sodium, 2 mg/kg;
gentamyacin, 3 mg/kg). Buprenorphrine was administered 3 and 12 h
after implantation to minimize pain. The animals' rectal temperature,
eating habits, and behavior were monitored daily. These measures
indicated that the goats were in normal good health by at least the 4th
day after surgery.
Methods of measurement. In the goats without a tracheostoma, a tight-fitting custom mask was taped to the snout, and a two-way breathing valve was attached to the mask. In the goats with a tracheostoma, a cuffed tracheostomy tube (7.6 mm ID) was inserted into the trachea, the cuff was then inflated, and the tube was connected to a two-way breathing valve. Inspiratory airflow was measured by a pneumotachograph attached to the inspiratory side of the breathing valve. The pneumotachograph was connected via tubing to a differential pressure transducer. The proximal ends of the EMG wires were connected via microclips to a Grass recorder for signal processing and recording on paper. The EMG signals were filtered at a band pass of 3-500 Hz. The airflow and raw EMG signals were sent for display, digital recording, and analysis to a CODAS computer data-acquisition system at a sampling rate of 250 Hz.
Experimental design. Before any data collection, the goats were thoroughly familiarized with all aspects of the experimental condition. At least 21 days after the initial surgery, the goats were monitored during wakefulness under eupneic and hypercapnic conditions. Six goats were also monitored while breathing room air during sleep. At least 14 days after implantation of MTs, a similar period of data collection was performed during wakefulness and sleep when no injections were performed. Even though they were in apparent good health, previous studies had shown that ventilation, arterial blood gases, and rectal temperature were not stable or at control levels until 10-14 days after brain surgery (8, 27).
On or after the 15th day after brain surgery, mCSF and subsequently 100 mM N-methyl-D-aspartic acid (NMDA; mixed in mCSF) were unilaterally microinjected (100 nl) through the MTs and into the tissue. The mCSF injection was intended as a control injection, whereas the agonist NMDA was injected to indicate whether neurons at the injection site were part of the respiratory or swallowing neural circuitry. It has been previously shown that this concentration of NMDA is effective in awake goats (8, 27). During these studies, respiratory airflow, EMG activity, heart rate, and arterial blood pressure were continuously monitored over an initial 15-min control period and for the subsequent 2-3 h. Injections were made at 30-min intervals, except when additional time was needed to fully recover from the previous injection. Over several subsequent days, mCSF, 250 mM kynurenic acid, 5 mM 2-amino-5-phosphonovalerate, or 0.3 mM 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo-(f)quinoxaline (NBQX) was microinjected (100 nl) unilaterally. These antagonists (each mixed in mCSF) have been shown to be effective in awake goats for several minutes after injection, thus creating a prolonged period of altered neuronal function (10, 27). The rationale for injections of different EAA-receptor antagonists was as an attempt to distinguish between NMDA- and non-NMDA-receptor contribution to the control of breathing and swallowing and their interaction. At least 4 h were allowed for recovery before a microinjection was made in the contralateral MT. The order of antagonist injections was randomized. In the hypercapnia studies pre- and post-MT implantations, CO2 was increased every 5 min by 2.5% to a maximum of 7.0% inspired CO2 fraction. In the injections studies, the hypercapnia was initiated 15 min after the injection.Sleep staging.
Sleep was assessed via EEG and/or EOG standard criteria and/or
behavioral criteria (9, 19, 20). The awake state was defined as low-voltage, mixed-frequency EEG with concurrent behavior of
head holding, alerting response to random ambient noises, and eye
blinks. Slow-wave sleep (SWS) was defined as a synchronized, low-frequency EEG (
2 Hz) with an amplitude two to three times greater
than that found during wakefulness and a concurrent absence of REM. REM
sleep was defined as a low-voltage, mixed-frequency desynchronization
of the EEG with frequent REM in the EOG channels and postural muscle
atonia indicated by an inability of head holding. REM sleep was also
associated with frequent twitching movements of the nose, ears, and
lips. The distinction between eye movements and blinks was made during
the control period by snapping fingers right and then left (eye
movements) and by lightly touching the goat's eye lashes to cause eye
blinks. Eye movements were associated with two to three times greater
change in voltage compared with eye blinks. Only measurements taken
during unequivocal wakefulness, SWS, and REM were analyzed.
Data analysis. Respiratory airflow and EMG signals were processed and analyzed (WinDaq, DATAQ Instruments). Raw EMG data were full-wave rectified and passed through a moving time averager (time constant of 0.1 s) to obtain an integrated EMG signal. The integrated EMG signal from the thryopharyngeus (TP) was analyzed to obtain the occurrence and rate of swallowing.
A FBr event was identified by three or more brief interruptions (40-150 ms) in EMGDia activity that were not associated with multiple swallows, mastication, vocalization, eructation, or movement artifacts. A lower limit of 40 ms was chosen because of limitations imposed by the sampling rate of the recordings. An upper limit of 150 ms and three or more interruptions were chosen because nearly all of the FBr fit these criteria. If a single swallow occurred after two or more brief interruptions in EMGDia activity, it was taken to signal the end of a FBr event. After a FBr was identified, the peaks of the integrated EMGDia signal were manually marked for six breaths immediately before the FBr, each peak during the FBr, and for six EMGDia peaks after the FBr (Fig. 1). From these markings, we calculated the onset interval, the average interval between EMGDia peaks during the FBr (FBr interval), the duration of the FBr (FBr duration), the number of FBr peaks (FBr peaks), the interval from the FBr to first EMGDia peak after the resumption of normal breathing (offset interval), and the average post-FBr breathing interval (post-FBr).
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Statistical analysis. To test whether the diaphragmatic and airflow parameters were significantly different from pre-FBr event values, a Student's t-test was used to compare the means of the percent values to 100% (i.e., no change; P < 0.01). To test whether the percent values during eupnea and hypercapnia were significantly different in the pre-MT and post-MT groups, a one-way ANOVA was used on the normalized diaphragmatic and airflow parameters (P < 0.02). In the subsequent post hoc comparisons, a Bonferroni t-test was applied to test whether the normalized data were significantly (P < 0.01) different between conditions.
Assessment of MT location. After the death of the goat (Beuthanasia), the brain was perfused with phosphate-buffered saline (pH 7.3) and 4% paraformaldehyde fixative and then removed. Frozen, transverse sections (20 µm) were cut, stained (hematoxylin and eosin), and examined microscopically. The distal end of the MT lesion was used to establish the site of injection into the brain stem. These sites were then identified to lie in specific regions according to a goat brain atlas (5).
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Of the goats that were studied without MTs implanted into their
brain stem, only 22.2% (4 of 18) had FBr events. Only one of the goats
had FBr events during SWS sleep (animal 2, Table 1).
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A total of 35 goats were studied after implantation of MTs (including 6 that were studied without MTs). Of these goats, 40% (14 of 35)
demonstrated FBr events (Table 1). Additionally, in the goats with FBr,
78% (11 of 14) had one or more implantations into or near the facial
(FN), vestibular (VN), or raphe nuclei (RN) that resulted in FBr (Fig.
2). In contrast, only 38% (8 of 21) of
the goats that did not demonstrate FBr had one or more implantations
into or near the FN or VN. Four goats that did not have FBr events
before implantation of MTs had FBr events after implantation. For all
goats after implantation of MTs, the rate of FBr events during
hypercapnia (17.2 ± 11.1 per hour) was not significantly
different (P > 0.01) from eupneic conditions
(14.5 ± 14.4 per hour). The same goat (animal 2, Table
1) that had FBr events during SWS before implantation of MTs also had
FBr during SWS after implantation.
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Characteristics of fractionated inspiration.
Figure 3 presents a representative FBr
event in an awake goat demonstrating a discharge pattern in the
diaphragm, a pharyngeal constrictor (TP) and a laryngeal dilator
[posterior cricoarytenoid (PCA)], and inspiratory airflow. At this
rate of fractionations during a FBr event, activations of PCA are in
phase with activations of the diaphragm. In contrast, pharyngeal
constrictor discharges occur during the off phase (expiratory) of the
inspiratory discharges. At higher rates of diaphragm fractionations
during a FBr event, TP activity was typically absent (not shown). In
addition, the typical postinspiratory activity of the diaphragm was
absent during FBr events. However, late expiratory activity was
maintained in the single goat in which the transversus abdominus was
monitored during FBr events (Fig. 4).
These observations demonstrate that FBr are short, although complete,
respiratory cycles with inspiratory followed by expiratory muscle
activity.
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Fractionated inspiration during sleep.
FBr as observed by others during REM sleep (15, 19, 20)
was also observed in goats (Fig.
5A). This REM-related FBr was characterized by a very irregular pattern of inspiratory diaphragmatic activity and airflow. At the same time, we frequently observed fractionated discharge patterns in the laryngeal abductors (PCA) and
adductors (thyroarytenoid) that were reciprocally out of phase but
clearly not associated with the phasic discharges in diaphragm activity. In contrast, the very regular patterned discharges of the
diaphragm and upper airway muscles during FBr events were not observed
during REM sleep in this study.
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Swallowing associated with FBr events. In all goats with FBr, a swallow occurred at the termination of or in the first breath after FBr in 60% of the FBr events (data not shown). The percentage of FBr events that was associated with swallows was not altered (P > 0.10) by implantation of MT or by switching from eupnea to hypercapnia. The characteristics of the FBr were not different (P < 0.05) between FBr that were not associated with swallows and those associated with swallows.
Effects of injections on FBr events.
The rates of FBr events, but not the FBr characteristics, were altered
in most goats by injections of mCSF or EAA-receptor agonist and
antagonist injection. Injections into the FN with mCSF produced either
no appreciable change (3 of 7 goats) or 
50% reduction (4 of 7 goats)
in the rate of FBr events during eupnea (Table
6). One goat (no. 7) demonstrated a 276%
increase after mCSF injections that was also associated with a 400%
increase in FBr events during hypercapnia. In contrast, the primary
response to hypercapnia in the remaining goats was an absence of FBr
events (5 of 7 goats). After NMDA injections into the FN, there was
either an absence (4 of 7 goats) or a substantial reduction (3 of 7 goats) of FBr events. Both the selective NMDA-receptor antagonist
2-amino-5-phosphonovalerate and the nonselective NMDA-receptor
antagonist kynurenic acid produced mixed results in the rate of FBr
events during eupnea and stimulated breathing (Table 6). However,
during eupnea, NBQX injections in FN either produced an approximately
twofold increase in FBr events (4 of 7 goats) or eliminated them
completely (3 of 7 goats). In the four goats with a twofold increase in
FBr events during eupnea after NBQX injections, the rate of FBr events
during hypercapnia varied between goats. The diaphragmatic and airflow
parameters were not significantly different (P > 0.05)
after EAA-receptor agonist or antagonist injections into FN during
eupnea or stimulated breathing.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study presents evidence of FBr during wakefulness and NREM sleep characterized by coordinated diaphragm and upper airway muscle activity and airflow, resulting in short, complete inspiratory-expiratory cycles. The breaths immediately after a FBr did not differ from pre-FBr breaths. Implantation of MTs into FN, VN, or RN regions of the brain stem increased the frequency of FBr, and microinjection of different substances at these sites altered the frequency of FBr events. Swallows were associated with the termination of, or the first breath after, the FBr. Finally, the FBr phenomenon was robust, as it did not differ between room air and hypercapnic conditions.
Neurophysiological basis for FBr events. Previous examples of FBr came from the research during REM sleep (19, 20) and with the acoustic startle reflex (15). In both of these areas of research, a FBr consisted of a 20- to 100-ms pause in diaphragm activity. During REM sleep, these pauses or fractionations are associated with PGO waves and often occur in a train of events. As part of an alerting response, the startle reflex is also associated with PGO waves and brief pauses of diaphragm activity but, in contrast to REM sleep, is usually a solitary event. The FBr events that we observed were unlikely caused by the same mechanisms as for REM sleep and an acoustic startle reflex because they were 1) different in pattern from the FBr found in REM sleep (Fig. 5 and Refs. 15, 19), 2) spontaneous and not associated with acoustic stimuli (14), and 3) not associated with PGO waves.
The FBr in goats were not associated with other behaviors that elicit changes in breathing pattern such as movement, regurgitation, coughing, rapid swallowing, gasping, vocalization, panting, or sniffing. Of these behaviors, the FBr in goats resembled the pattern of diaphragm activity observed with sniffing. Mechanical stimulation of the nasopharynx (1) or epipharynx (26) in anesthetized animals or presentations of a noxious odor in unanesthetized rabbits (6) elicit a sniff or an aspiration reflex. In these experiments, trains of rapid bursts of diaphragm activity are produced at an approximate rate of 5 Hz (similar to what was seen in this study). The study by Batsel and Lines (1) and Tomori and Widdicombe (26) involved glossopharyngeal or vagal-medullary reflexes, and the study by du Pont (6) involved afferents from the olfactory system. Several studies examined respiratory-related neurons in the medulla during induced sniffs. In cats, Batsel and Lines (1) observed with the increased inspiratory-related neuronal activity an "inhibition or disfacilitation" of expiratory neurons during induced sniffing. In contrast, during sniffing, du Pont (6) observed reciprocal activation of inspiratory and expiratory neurons, even though expiration was nonfunctional and, consequently, lung volume increased. Chang (4), in unanesthetized guinea pigs, observed a series of short, rapid bursts in diaphragm activity during phonation (chirping; 15-30 Hz) and spontaneous sniffing (5-15 Hz). In this later study (4), a higher frequency of diaphragmatic bursts during phonation was associated with an increased firing of inspiratory neurons within para-ambigual nuclei and an inhibition or disfacilitation of the expiratory neurons of the Bötzinger complex. At the slower rate observed during sniffing, both the inspiratory related neurons in the region of the para-ambigual nucleus and the expiratory-related neurons were reciprocally activated, demonstrating short, complete inspiratory-expiratory cycles. The above studies provide insights into changes in medullary neuronal activity during sniffing and phonation. Even though the FBr in awake goats were not associated with sniffing and phonation, the FBr in goats resembled the pattern of these behaviors. It thus seems reasonable to consider that the FBr in goats was due to perturbation of a medullary neuronal network.MT implantation and EAA-receptor agonist and antagonist injections. The marked increase in the incidence of FBr with the placement of the MTs in and around the FN, VN, and RN suggests that these areas are involved in the genesis of the FBr. Apparently, the lesion created by implanting the MT was sufficient to increase FBr frequency. In addition, subsequent injection of mCSF and EAA-receptor agonist and antagonist at these sites altered the frequency of FBr. The greatest changes were found after injection of the antagonist NBQX, which indicates that non-NMDA receptors are probably involved in the mechanism of the FBr. However, because implantations alone and injections of mCSF affected the frequency of the FBr, it seems that there was primarily a nonspecific effect at these three nuclei. On the other hand, the effects of the implantation and the injection do not appear due to nonspecific perturbation of the reticular activating system, because perturbations at several other medullary sites did not alter the frequency and characteristics of the FBr. These findings thus suggest that perturbation of medullary neurons or a neuronal network underlies FBr in awake goats.
Mechanism of FBr in awake goats. The frequency and characteristics of the FBr in awake goats did not differ between room air and a hypercapnia-induced hyperpnea. This finding indicates that the FBr phenomenon is "robust" and not readily eliminated. Moreover, the finding suggests that the FBr phenomenon is not another form of periodic or irregular breathing, because many forms of these breathing patterns are eliminated or reduced by hypercapnia (2, 13, 17).
Swallows occurred at the end of, or in the first breath after, 60% of the FBr. Inspiratory swallows are known to cause brief interruptions in diaphragm activity and airflow in goats (7). However, a single inspiratory swallow did not cause a FBr event, because, by definition, the FBr included three or more interruptions in inspiration not associated with swallows. In addition, swallows are thought to have a general inhibitory effect on breathing (7, 16). Conceivably, this general inhibition of swallowing on breathing was too brief or weak to initiate a swallow, and/or there was a delay in the onset of the swallow. As a result, a series of brief, small breaths occurred until the inhibition strengthened to permit a swallow. Because ~40% of the FBr were not associated with swallows and because the characteristics of the FBr did not differ between FBr associated and not associated with a swallow, other mechanisms need to be considered as causes of the FBr. Another potential clue relative to the mechanism of the FBr is that the interval between the peak diaphragm activity of the breath preceding the FBr and the first peak diaphragm activity of the FBr was 15-20% shorter than the average interval of the preceding breaths. This finding implies activation of a motor program different from normal. Interesting though is that the breath duration of the first five breaths after a FBr did not differ from the breath duration before the FBr, indicating that the FBr are a transient, distinct phenomenon. It is thus conceivable that an ectopic or anomalous rhythm generator transiently "overrides" the normal respiratory rhythm generator or that the normal generator transiently increased its rate. Or, as suggested by others (4,6), FBr may be a result of the entrainment of respiratory neurons outside of and/or downstream from the respiratory rhythm generator. The activation of sniffing by stimulation via glossopharyngeal, vagal, and olfactory afferents suggests that these afferents may modulate this neuronal network. This latter point is supported by findings that neurons in the rostral medulla supposedly function as a network to integrate stimuli from many different sources (4, 8, 22, 23, 25). Also relevant are observations that some of the swallowing-related neurons receive respiratory-related inputs. That is, neuronal networks involved in respiration may also receive input from networks that are involved in behaviors such as swallowing, sniffing, and phonation. This interpretation is in line with the concept that a common set of motoneurons is driven by both swallowing and breathing central pattern generators (11, 12, 18, 21).Conclusions. The five key findings relevant to the mechanism of the FBr events are as follows: 1) the duration of neural expiration before the FBr was shorter than during normal respiratory cycles; 2) the five breaths before and after the FBr did not differ; 3) the lack of difference in rate and characteristics of FBr events between eupnea and hypercapnia; 4) the large percentage of FBr events terminated with a swallow; and 5) the altered frequency of FBr after nonspecific perturbations within the FN, VN, and RN. We speculate that FBr events manifest the disruption of a medullary neuronal network that includes the FN, VN, and RN, which is responsible for the coordination of breathing with the numerous other behaviors utilizing the same anatomic structures. This hypothesis is consistent with our previous findings that perturbations of neuronal function of rostral medullary nuclei disrupt the coordination of breathing and swallowing (8). Alternatively, FBr events may reflect transient changes in synaptic inputs that increase the rate of the normal rhythm generator or allow an ectopic, anomalous generator to become dominant.
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ACKNOWLEDGEMENTS |
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The authors thank Dr Edward H. Vidruk for review and critique of this manuscript. In addition, we thank Dan Brozoski, Leanne Klum, and Alex Serra for assistance in acquiring the data and in the preparation of the manuscript.
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FOOTNOTES |
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This study was supported by National Heart, Lung, and Blood Institute Grant HL-25739 and the Department of Veterans Affairs.
Address for reprint requests and other correspondence: H. V. Forster, Medical College of Wisconsin, 8701 Watertown Plank Rd., Milwaukee, WI 53226 (E-mail: bforster{at}mcw.edu).
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.
10.1152/japplphysiol.00837.2002
Received 13 September 2002; accepted in final form 19 November 2002.
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TOP
ABSTRACT
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METHODS
RESULTS
DISCUSSION
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I) was partitioned
into inspiratory time (TI), expiratory time
(TE), and tidal volume for the 5 breaths before, during,
and 5 breaths after a FBr event. The intervals between peak diaphragm
activity for 5 breaths before, during, and 5 breaths after the FBr
event were also calculated. DiaMTA, moving time average
(MTA) of diaphragm (Dia) electromyogram (EMG); Raw, raw EMG; Intv,
interval.
, The locations of the MT in goats with FBr events;
, the locations of MT in goats without FBr events. FN,
facial nucleus; FNl, facial nucleus lateral division; FNm, facial
nucleus medial division; RGN, gigantocellularis reticularis; VN,
vestibular nucleus; R, raphe nucleus; HP, hypoglossal propositus; RB,
restiform body; 5SP, spinal trigeminal nucleus; 5ST, spinal trigeminal
tract; P, pyramids; CON, cochlear nucleus; NTS, nucleus tractus
solitarius; TS, tractus solitarius; DMV, dorsal motor nucleus; FTL,
lateral tegmental field; IO, inferior olivary nuclei; NA, nucleus
ambiguus; CN, cuneate nucleus.
