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Department of Pediatrics, Robert Wood Johnson Medical School, University of Medicine and Dentistry of New Jersey, New Brunswick 08903; and Department of Biomedical Engineering, Rutgers, The State University of New Jersey, Piscataway, New Jersey 08854
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The hypothesis that respiratory modulation due to upper airway (UA) pressure and flow is dependent on stimulus modality and respiratory phase-specific activation was assessed in anesthetized, tracheotomized, spontaneously breathing piglets. Negative pressure and flow applied to the isolated UA at room or body temperature during inspiration only enhanced posterior cricoarytenoid muscle activity from that present without UA pressure and flow (baseline) by 15-20%. Time shifting the onset of UA flow relative to tracheal flow decreased this enhancement. The same enhancement was observed with oscillatory or constant airflow. UA positive pressure and flow at room or body temperature applied during expiration only enhanced thyroarytenoid muscle activity from baseline by 50-160%. The same enhancement was observed with oscillatory or constant airflow at body temperature. Constant positive pressure and flow enhanced thyroarytenoid muscle activity more than oscillatory pressure and flow at room temperature. We conclude that the respiratory modulation of UA afferents is processed in a phase-specific fashion and is dependent on stimulus modality (tonic vs. phasic).
control of breathing; posterior cricoarytenoid; thyroarytenoid; larynx; reflexes; piglet
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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UPPER AIRWAY (UA) pressure- and flow-sensitive endings have been identified in the larynx, supplied mainly by the internal branch of the superior laryngeal nerve of the vagus (19); in the nasopharynx, supplied by the glossopharyngeal nerves (28); and in the nasal mucosa, supplied by the ophthalmic and maxillary divisions of the trigeminal nerve (21, 25, 27). In the accompanying study (24), we showed that presumably stimulating these receptors with pressure and flow in the isolated UA modulates the phasic respiratory activity of intrinsic laryngeal muscles. Our results showed that the phasic respiratory activity of the posterior cricoarytenoid muscle (PCA), a laryngeal abductor, above tonic levels is enhanced by the presence of UA negative pressure and inspiratory flow during inspiration. Increased abduction during inspiration widens the glottic opening and decreases resistance to airflow (4, 5). We also showed that phasic respiratory activity of the thyroarytenoid muscle (TA), a laryngeal adductor, is enhanced by UA positive pressure and expiratory flow during expiration. Phasic expiratory activity of the TA adducts or narrows the vocal folds, resulting in increased resistance to airflow out of the lungs (5, 12).
The firing characteristics of UA pressure- and flow-sensitive endings have been extensively characterized. "Flow" receptors actually function as thermoreceptors, stimulated by cooling of the UA mucosa from body temperature to room temperature (19). Laryngeal pressure and flow receptors have slowly adapting discharge, similar to mechanoreceptors with vagal afferents in the lungs, and also show a dynamic sensitivity (14, 20). These receptors can be stimulated continuously with a tonic stimulus or, for a short period of time, with a phasic stimulus.
Woodall et al. (29) showed that phasic laryngeal dilator activity was enhanced by negative pressure pulses applied to the isolated UA during early inspiration, whereas it remained unaffected by late applications. These results suggest that UA afferent information is processed in a phase-specific fashion, analogous to afferents conveying lung stretch feedback (11) or peripheral chemoreception (3).
To evaluate the contribution of UA receptors sensing pressure and flow to the controlled respiratory phase-specific activation of laryngeal muscles, we studied the effects of application of airflow at room or body temperature to the isolated UA of anesthetized, tracheotomized, spontaneously breathing piglets to presumably stimulate specific receptors (flow and/or pressure) in a tonic (constant) or phasic (oscillatory) fashion. Altering the temperature of the air applied to the isolated UA presumably allows for recruitment of pressure receptors only or both pressure and flow receptors. We assessed the phase dependency of reflex responses of laryngeal abduction to UA pressure and flow by introducing varying time delays between the onset of UA pressure and flow relative to tracheal pressure and flow. We hypothesized that, analogous to lung mechanoreceptor feedback, afferent information from UA pressure and flow receptors is dependent on stimulus modality (tonic vs. phasic) and is processed centrally in a phase-specific fashion.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The protocol was approved by the Institutional Animal Care and Use Committee at the Robert Wood Johnson Medical School.
Surgical preparation.
Twenty-two piglets of either gender (15.8 ± 2.1 days of age,
range 3-33 days; 3.97 ± 0.30 kg body wt) were prepared as
described in the accompanying study (24). Some data were
collected from the same piglets prepared for that study
(24). Briefly, piglets were premedicated for surgical
preparation with acepromazine (1 mg/kg im) and ketamine (45 mg/kg im).
A few drops of Xylocaine (2% lidocaine HCl, 20 mg/ml sc) or a topical
anesthetic skin refrigerant (ethyl chloride) was used to premedicate
areas before incisions. Animals were anesthetized with a constant
infusion of ketamine (
0.3
mg · min
1 · kg1 iv as
required to maintain anesthesia). Animals were tracheotomized and
allowed to breathe spontaneously. A differential pressure transducer
(Validyne) and a pneumotachograph (Hans Rudolph) connected to a
transducer (Validyne) were attached to monitor tracheal flow and
pressure, respectively. The rostral segment of the trachea was
intubated below the larynx and attached to a pneumotachograph (Fleisch)
connected to a differential pressure transducer (Validyne) for
measurement of UA flow and a differential pressure transducer (Validyne) for measurement of UA pressure.
Isolated UA breathing circuit. The UA was isolated, and a breathing circuit was constructed for the generation of oscillatory pressure and flow, with air at room temperature or warmed to 40°C by passage through coiled tubing submerged in a temperature-controlled bath to achieve body temperature when the air passed through the UA.
Tracheal flow during inspiration was used to command a servo-controlled valve (1) connected to the isolated UA. Tracheal inspiration resulted in concomitant opening of the valve, which exposed the larynx to a negative pressure source, pulling bias air available at the snout in the inspiratory direction, concomitant with tracheal inspiration. Closure of the valve (triggered by the lack of inspiratory tracheal flow) resulted in the absence of UA pressure and flow. Locking the valve in the open position resulted in constant negative pressure and inspiratory flow (see Fig. 1A of Ref. 24). Alternatively, tracheal flow during expiration was used to command opening of the servo-controlled valve, exposing the larynx to a positive pressure source, which pushed air in the expiratory direction, concomitant with tracheal expiration. Locking the valve in the open position resulted in constant positive pressure and expiratory flow (see Fig. 1B of Ref. 24). Maximum oscillatory or constant UA negative pressure was
9.8 ± 0.7 cmH2O, whereas maximum oscillatory or constant UA
positive pressure was 9.2 ± 0.5 cmH2O, resulting in
UA flows of 0.5 l/min.
To introduce varying time delays between the onset of UA oscillatory
pressure and flow and tracheal pressure and flow (Fig. 1), we designed and implemented a
microelectric circuit consisting of a series of three all-pass constant
time-shifting active filters (2nd-order Bessel filters) and amplifiers.
The circuit allowed us to phase shift the animal's inspiratory
tracheal flow signal used to command the UA breathing circuit valve.
Cycle shifting was set at 25, 50, 75, and 100% of the inspiratory time
for UA negative pressure and flow through the isolated UA. PCA EMG
activities and ventilatory measurements were compared at different
phase-shifting levels relative to the absence of UA pressure and flow.
Because of the shape of the expiratory tracheal pressure and flow
waveform (end-expiratory pauses), we were unable to phase shift UA
expiratory pressure and flow without considerable signal distortion.
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Data collection and analysis. Data were recorded on chart paper (model TA 4000, Gould) and digital tape (model 4000A, Vetter). Pressure, flow, and EMG MTA data were digitized at a sampling rate of 25 Hz for computer-assisted analysis on-line on a desktop microcomputer fitted with data-acquisition hardware and storage (CODAS, DATAQ). EMG activities were quantitated as the peak height of the phasic MTA activity above tonic levels during inspiration (PCA and Dia) or expiration (TA and Abd). Ventilatory parameters [inspiratory (TI), expiratory (TE), and total respiratory time (TT) and tidal volume (VT)] were measured or calculated breath by breath using data-acquisition software (Advanced CODAS, DATAQ). TI was defined as the time from the onset to maximum phasic activity of the MTA Dia EMG above tonic levels for each breath. TE was defined as the time from the maximum level of phasic MTA Dia EMG above tonic values to the onset of the subsequent breath. TT was defined as the sum of TI and TE. VT was calculated by digital integration of tracheal flow records. Additional calculations were performed with spreadsheet software (Quattro Pro for Windows, Borland).
Responses obtained during control or baseline conditions were calculated as an average of values obtained in 20 breaths before the application of each pressure and flow stimulus to the isolated UA. Stimulus values were computed as an average of values corresponding to 20 consecutive breaths. The first 10 breaths following the application of the stimulus were excluded to avoid pressure and flow artifacts due to opening and closure of the servo-respirator valve and to allow for attainment of a steady-state response. Changes in parameters were quantified as percent changes from control parameters. Statistical differences in parameters obtained under stimulus conditions were assessed by ANOVA and t-test. Whenever normality and equal variance tests failed, nonparametric statistics (sign test, rank-sum test, ANOVA on ranks) were used instead to interpret results. The chosen level of significance was P < 0.05. Maturational changes were assessed by computing the Pearson correlation coefficient for the measured respiratory variables vs. age, and significance was assessed by the calculated probability value. Values are means ± SE. Tests were conducted using computer software for statistical analysis (SigmaStat, Jandel Scientific).| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Oscillatory vs. constant UA negative pressure and inspiratory flow.
Figure 2 illustrates the typical pattern
of responses observed when the effects of tonic and phasic UA negative
pressure and flow are assessed. Constant pressure and flow presumably
stimulate slowly adapting receptors continuously, whereas oscillatory
pressure and flow stimulate these receptors for a short period of time. Figure 2 shows that oscillatory and constant negative pressure and
inspiratory flow applied to the isolated UA enhance PCA EMG activity,
whereas Dia and Abd activity remain unaffected.
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3.2 ± 1.0%). Respiratory timing was assessed in 10 piglets. Increases in TT were significant for room and body temperature oscillatory airflow (3.3 ± 0.9 and 3.0 ± 0.7%,
respectively), as well as for room temperature constant airflow
(3.4 ± 1.8%), whereas TE increased significantly
with body temperature oscillatory flow only (3.1 ± 1.6%). Abd
activity remained unchanged from baseline values under all conditions
tested. Our results did not reveal significant age differences in the
respiratory response to oscillatory or constant UA negative pressure
and inspiratory flow.
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Oscillatory vs. constant UA positive pressure and expiratory flow.
Figure 4 illustrates the typical pattern
of responses observed when the respiratory effects of oscillatory and
constant positive pressure and expiratory flow are assessed.
Oscillatory positive pressure and expiratory flow increased peak phasic
MTA TA EMG from baseline values, whereas Dia and Abd activity remained
unaffected. The degree of enhancement of TA activity with constant
pressure and flow is greater than that obtained with oscillatory
positive pressure and expiratory flow applied to the isolated UA during expiration only.
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Phase-shifted UA negative pressure and inspiratory flow.
The effect of altering the temporal relationship between UA negative
pressure and inspiratory flow on average peak phasic MTA PCA activity
was studied in 12 piglets. Enhancement was obtained at all tested phase
shifts: 25, 50, 75, and 100% relative to the absence of UA pressure
and flow. Not all phase shifts were available in all animals studied.
To establish a balanced design, shifting was binned at 0, 25-50,
and 75-100%, as shown in Fig. 6.
Values for the three bins were available in 10 piglets (15.3 ± 3.2 days of age, range 5-33 days; 3.92 ± 0.45 kg body wt). A
statistically significant difference between the groups was observed
(ANOVA). The enhancement of PCA activity diminishes with increasing
phase shifting.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The novelty of our findings is in our assessment of the
steady-state respiratory response of piglets to UA pressure and flow, with profiles that resemble those present during eupneic breathing (with pressure and flow oscillating during inspiration or expiration at
the respiratory frequency of the animal). We have shown in the
accompanying study (24) that the respiratory modulation of
UA pressure and flow is characterized by an enhancement of laryngeal
abduction during inspiration and adduction during expiration, while
respiratory pump muscle activity remains relatively unaffected. In the
present study, we investigated the effects of different stimulus
modalities (tonic or phasic) on the presumable activation of UA
pressure and flow receptors. The existence of slowly adapting pressure
and flow receptors, capable of exhibiting a high dynamic sensitivity, assessed by the single-unit superior laryngeal nerve afferent fiber recording study of Sant'Ambrogio et al.
(19) suggests that the reflex response to laryngeal
receptor stimulation could be affected by stimulus modality. Our
results showed that the presumable stimulation of UA receptors with a
constant or oscillatory stimulus enhanced phasic PCA and TA EMG
activity. With room temperature air, enhancement of TA EMG activity was greater with constant UA pressure and flow than with oscillatory UA
pressure and flow, suggesting that UA flow receptors are not stimulated
as much with a phasic stimulus as with a tonic stimulus. In all other
test conditions, oscillatory or constant UA pressure and/or
flow resulted in the same degree of enhancement of PCA or TA EMG
activity. We conclude that the reflex enhancement of laryngeal
abduction and adduction with UA pressure and flow is mainly
attributable to tonic stimulation of UA receptors. Although the
observed changes in Dia EMG activity with UA negative pressure and
oscillatory flow (3.2% from baseline) and with UA positive pressure
and oscillatory flow (3.4% from baseline) at room temperature are
statistically significant, we consider them to be not physiologically relevant in relation to the observed enhancement of PCA activity (15-20% from baseline) and TA activity (50-160% from
baseline) with oscillatory and constant UA pressure and flow.
The effect of UA pressure on the control of breathing in humans and
animals has been extensively characterized via a variety of approaches.
One approach is to compare the effects of nasal and tracheal occlusion
tests (during nasal occlusion, the UA is subjected to pressure change
induced by contraction of the thoracic pump muscles). This approach was
used in unanesthetized dogs in the study of Issa et al.
(9), which concluded that UA mechanoreceptors may
facilitate induction of arousals during sleep, and in the study of
Eastwood et al. (2), which found that UA occlusions decreased the rate of rise of Dia activity while increasing the activity of UA dilator muscles. Another way to stimulate UA
mechanoreceptors is with pressure pulses: Horner et al.
(8) applied 25-cmH2O pressure and found
reflex activation of the human genioglossus muscle.
Although most studies have examined the respiratory effects due to application of static or pulse pressures, the effects due to oscillatory pressures have also been investigated (6, 7, 16). These studies used a 30-Hz oscillating frequency to simulate that during human snoring, which resulted in increased genioglossus activity in sleeping dogs (16), increased incidence of arousal in sleeping humans with central apneas (6), and increased Dia and genioglossus EMG activity during sleep in normal humans and in humans with sleep apnea (7).
The approaches mentioned above give insights into the effects of
presumably stimulating UA mechanoreceptors; however, the use of an
isolated UA preparation such as ours eliminates the concomitant effect
of also stimulating mechanoreceptors found elsewhere in the airways.
Janczewski (10) found that application of
30-cmH2O pressure pulses to the isolated larynx of
rabbits enhanced genioglossus muscle activity, as well as phrenic,
hypoglossal, and facial nerve activity. The effect of application of
static positive or negative pressure to the isolated UA on abdominal muscle activity was assessed by the study of Plowman et al.
(17), which found a short-latency, transient decrease in
Abd EMG, which subsequently recovered to baseline activity during
application of the stimulus in conscious dogs.
The respiratory effects of UA flow or cooling receptor stimulation have also been assessed. Zhang and Bruce (30) compared the effects of room and body temperature static airflows applied to the isolated UA of anesthetized rats and found that Dia activity is depressed with room temperature, but not with body temperature, airflows. In their preparation, negative pressures (10-14 cmH2O) applied against an occluded nose and mouth increased genioglossus and PCA EMG activity, whereas positive pressure decreased genioglossus EMG activity.
Our approach differs from those mentioned above, in that we applied pressure and flow stimuli to the isolated UA in magnitude comparable to that present during eupnea, which minimized the response of respiratory pump muscles while revealing effects on laryngeal muscle activity. Application of pressure and flow profiles to the UA that resemble those generated by the animal's tracheal respiration, at the same respiratory frequency of the animal, allowed us to presumably activate UA pressure and flow receptors in a phasic fashion resembling that present during eupneic breathing. Furthermore, varying the temperature of the airflow applied to the UA allowed us to separate the effects of presumably stimulating UA pressure receptors only or both pressure and flow receptors.
The UA pressure receptor population has been shown to consist mainly of those exhibiting slowly adapting firing characteristics (14). Conversely, UA flow receptors exhibit fast adaptation rates (20), suggesting that the reflexes can be attributed mainly to pressure receptor stimulation. This conclusion is consistent with the findings of the accompanying study (24) and the fact that, if the relative distribution of laryngeal receptors in the piglet is assumed to be similar to that in the dog, pressure-modulated endings account for the majority (~60%) of the respiratory-modulated receptor population described by Sant'Ambrogio et al. (19). However, although only 15% of pressure receptors are responsive to distending or positive pressure, the results of the studies of the effects of UA positive pressure and expiratory flow on TA activity suggest that this small receptor population is capable of producing a more pronounced reflex response than that observed on PCA activity due to stimulation of the dense UA negative pressure receptor population.
We are unaware of any studies that identified pressure and flow receptors in the UA of piglets. We chose to study piglets, because this model is very suitable to investigate maturational development of a variety of reflexes, given the size of the animals at birth and their growth rate within the first days and weeks of life. Our results did not reveal maturational differences in the reflex response to oscillatory and constant UA pressure and flow within the 1st mo of life of the piglet. On the basis of maturational changes in chest wall compliance (24), we predict that restricting studies to piglets within the 1st wk of life may reveal such differences.
Care should be taken in extrapolating findings from UA receptors in dogs, inasmuch as there is evidence of species differences in the relative distribution of pressure and flow receptors in the UA as well as in the response of these receptors to respiratory stimuli. For example, although flow receptors have been identified in the superior laryngeal nerve of dogs (20) and rabbits (15), they were not found in guinea pigs (26). Unlike laryngeal mechanoreceptors in dogs, the majority of pressure receptors in rats (22), guinea pigs (26), and rabbits (15) are stimulated by positive pressure and inhibited by collapsing pressure. The low percentage or lack of certain laryngeal receptors in some species may be compensated by the presence of receptors found elsewhere in the UA, such as in the nasal passages. Nasal pressure and cooling receptors have been identified in cats, rats, and guinea pigs (21, 23, 25, 27).
The respiratory response to a given stimulus can be dependent on the time of application of the stimulus within the respiratory cycle. Studies to produce UA pressure and flow out of phase with the onset of tracheal pressure and flow were designed to answer the question of whether timing of UA receptor feedback in relation to respiratory timing could affect the strength of the reflex response to receptor activation. The latter has been shown to be true for other respiratory-related feedback systems, such as peripheral chemoreceptors (3) and mechanoreceptors in the lung (11).
We hypothesized that, analogous to other respiratory-related
feedback systems, information from UA pressure and flow afferents would
also be processed in a phase-specific manner. Data from Woodall et al.
(29) supported our hypothesis. They showed greater enhancement of phasic genioglossus EMG activity with early (within the
first 200 ms) applications of negative pressure pulses during inspiration to the isolated UA than with late (200 ms) inspiratory application. The magnitudes of phasic EMG activity of the alae nasi and
PCA were enhanced by early negative pressure applications but
unaffected by late applications. These studies differ from ours, in
that we have shown the reflex response to a stimulus that better
represents the stimulus during eupnea (i.e., isolated UA pressure and
flow profiles similar to those generated by the animal) at distinct
points of the inspiratory cycle.
Our results showed the most pronounced enhancement of PCA activity with upper and lower airway pressure and flow in phase with each other. This suggests a protective mechanism to maintain UA caliber. Because stimulation of UA mechanoreceptors, regardless of stimulus modality, rarely affected respiratory pump muscle activity (Dia or Abd) while favoring enhanced laryngeal abduction, the resultant decrease in inspiratory UA resistance should lessen the load imposed on pump muscles. Similarly, inasmuch as laryngeal adduction is favored during expiration, increased expiratory UA resistance assists in braking of expiratory airflow, lessening the load imposed on chest wall muscles to achieve the same level of braking. The relevance of this neonatal breathing strategy to increase functional residual capacity above passive levels is discussed in the accompanying study (24).
Analogous to lung mechanoreceptor feedback, we have shown that afferent information from UA receptors is dependent on stimulus modality (tonic vs. phasic UA pressure and flow) and is processed centrally in a phase-specific fashion. We conclude that UA pressure and flow receptors play an important role in modulating phasic respiratory activity of intrinsic laryngeal muscles on a breath-by-breath basis.
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ACKNOWLEDGEMENTS |
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The authors thank Jianmin Chen for expert technical assistance during preliminary studies.
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FOOTNOTES |
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This study was supported by National Heart, Lung, and Blood Institute Grant HL-45520. M. H. Stella was a recipient of a Regular Training Program Fellowship from the Organization of American States and a predoctoral fellowship from the American Heart Association-New Jersey Affiliate.
Address for reprint requests and other correspondence: M. H. Stella, Dept. of Physiology, Dartmouth Medical School, One Medical Center Dr. Lebanon, NH 03756 (E-mail: martha.h.stella{at}dartmouth.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.
Received 31 August 2000; accepted in final form 3 April 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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  N. Samson, B. Roy, A. Ouimet, F. Moreau-Bussiere, D. Dorion, S. Mayer, and J.-P. Praud Origins of the inhibiting effects of nasal CPAP on nonnutritive swallowing in newborn lambs J Appl Physiol, October 1, 2008; 105(4): 1083 - 1090. [Abstract] [Full Text] [PDF]
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N. Samson, M. St-Hilaire, E. Nsegbe, P. Reix, F. Moreau-Bussiere, and J.-P. Praud Effect of nasal continuous or intermittent positive airway pressure on nonnutritive swallowing in the newborn lamb J Appl Physiol, November 1, 2005; 99(5): 1636 - 1642. [Abstract] [Full Text] [PDF]
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