J Appl Physiol 95: 22112217, 2003.
translational physiology
Lung volume effects on pharyngeal swallowing physiology
Roxann Diez Gross,1,2 Charles W. Atwood, Jr.,3
Judith P. Grayhack,1,2 and Susan Shaiman2
1
Department of Audiology and Speech Pathology and 3Pulmonary Section, Veterans Affairs Pittsburgh
Healthcare System, Pittsburgh 15240; and 2Department of Communication Sciences and Disorders,
School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
Submitted 27 March 2003; accepted in final form 7 August 2003
Gross, Roxann Diez, Charles W. Atwood, Jr., Judith
P. Grayhack, and Susan Shaiman. Lung volume effects on
pharyngeal swallowing physiology. J Appl Physiol 95:
22112217, 2003. First published August 8, 2003; 10.1152/
japplphysiol.00316.2003.The experiment was a prospec-
tive, repeated-measures design intended to determine how
the variation of lung volume affects specific measures of
swallowing physiology. Swallows were recorded in 28 healthy
subjects, who ranged in age from 21 to 40 yr (mean age of 29
yr), by using simultaneous videofluoroscopy, bipolar intra-
muscular electromyography, and respiratory inductance
plethysmography. Each subject swallowed three standard-
ized pudding-like consistency boluses at three randomized
lung volumes: total lung capacity, functional residual capac-
ity, and residual volume. The results showed that pharyngeal
activity duration of deglutition for swallows produced at
residual volume was significantly longer than those occur-
ring at total lung capacity or at functional residual capacity.
No significant differences were found for bolus transit time or
intramuscular electromyography of the superior constrictor.
The results of this experiment lend support to the hypothesis
that the respiratory system may have a regulatory function
related to swallowing and that positive subglottic air pres-
sure may be important for swallowing integrity. Eventually,
new treatment paradigms for oropharyngeal dysphagia that
are based on respiratory physiology may be developed.
deglutition; dysphagia; dynamic; subglottic mechanorecep-
tors; subglottic air pressure
DEGLUTITION, WHICH INCLUDES the physiological act of the
pharyngeal swallow, is necessary to sustain life. Res-
piration is also indispensable for survival. Interest-
ingly, these two important life-sustaining functions
must share crucial anatomic space, because the upper
airway serves as a common pathway for both air and
nourishment. Similarly, the brain stem neurons and
interneurons that control these functions are in close
proximity (44). To date, research efforts have focused
on the coordination of respiration and swallowing from
a turn-taking perspective, without consideration of a
more integrated paradigm whereby the respiratory
system and the airflow that it governs actively partic-
ipate in deglutition.
Address for reprint requests and other correspondence: R. D.
Gross, VA Pittsburgh Healthcare System, Dept. of Audiology and
Speech Pathology, University Drive C (132A-U), Pittsburgh, PA
15240 (E-mail: Roxann.Gross@med.va.gov).
http://www.jap.org
First published August 8, 2003; 10.1152/japplphysiol.00316.2003.
Subglottic Pressure Theory for Swallowing
The rationale for this study is based on the theory
that pressurized air during the swallow may play a role
in the neuroregulation of swallowing function by stim-
ulating subglottic mechanoreceptors. The subglottic
pressure theory for swallowing originated from obser-
vations of altered swallowing function in tracheostomy
patients in which air pressure below the true vocal
folds was greatly modified, depending on the status of
the tube (open or closed). The location of subglottic
pressure receptors has been verified (3, 48, 49), al-
though their function is not yet known (4, 13, 33, 42,
45, 46). Conceivably, the purpose of these receptors
may be related to deglutition and not phonatory or
respiratory function.
Tracheostomy Tubes and Aspiration
The placement of an indwelling, open tracheostomy
tube not only functionally separates the respiratory
and alimentary tracts but also eliminates the possibil-
ity of generating positive subglottic air pressure
(Psub). Increased aspiration and dysphagia have been
linked to the presence of an open tracheostomy tube
(68, 28, 29). Closure of the tracheostomy tube and
restoration of positive pressure can be achieved by
capping or digital occlusion or by placement of a Passy-
Muir speaking valve. Investigations that looked pri-
marily at head and neck cancer patients without neu-
rological impairment have reported that aspiration
was eliminated or reduced when the tracheostomy tube
was occluded during the swallow (11, 15, 43).
Additional evidence to support the importance of
Psub in swallowing function has also been offered in
the pediatric literature. Finder and colleagues (12)
reported that dramatic reductions in aspiration of sa-
liva were observed after the institution of constant
positive airway pressure (CPAP) through the open
tracheostomy tube. The authors speculated that there
was a relationship between the application of CPAP
and tracheostomy tube occlusion, but they did not
consider that CPAP may have actually improved swal-
lowing function by providing positive Psub during the
swallow while the tube remained open.
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.
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2212 LUNG VOLUME EFFECTS ON SWALLOWING
Respiration and Deglutition
There is overwhelming evidence that points to the
coupling of swallowing with the exhalation phase of res-
piration, but little explanation as to why this coordina-
tion exists (21, 24, 25, 38, 40). Perhaps the preferential
timing of the normal swallow with the exhalation phase
is a mechanism that allows for stimulation of subglottic
mechanoreceptors and the generation of the Psub that
seems to be missing when patients swallow with an open
tracheostomy tube. Conceivably, feedback mechanisms
that use afferent information from the subglottis may be
more readily accessed at higher lung volumes or during
exhalation when it is easiest to produce positive air pres-
sure. Additionally, individuals who suffer from neurolog-
ical injury have been shown to experience a disturbance
of coordination between respiration and swallowing (9,
38). A high incidence of dysphagia and aspiration has
been reported for this population as well (19, 31, 41).
Possibly, a loss of optimal coupling of the onset of the
swallow with higher lung volumes could result in a dis-
ruption of Psub. The disruption of requisite pressure may
be key to understanding the high incidence of dysphagia
and aspiration within neurologically impaired individu-
als and other diagnostic groups.
This experiment was designed to determine how the
variation of one easily manipulated respiratory param-
eter, lung volume, affects specific measures of swallow-
ing physiology in individuals without dysphagia, respi-
ratory disease, or neurological impairment. Extremes
in lung volume were used as a means to alter subglottic
air pressure in individuals who do not have indwelling
tracheostomy tubes.
METHODS
The protocol was approved by the Veterans Affairs Pitts-
burgh Healthcare System Subcommittee on Human Studies
and the Institutional Review Board of the University of
Pittsburgh. Informed written consent was obtained from
each participant before data collection.
Sample
Before data collection, a power analysis based on a power
of 0.70 at a 0.05 level of significance determined that 25
subjects would be required for a medium effect size. Due to
anticipated data loss, 28 subjects were recruited.
Participants
The participants were 28 healthy, young volunteers re-
cruited from the general population. The age range of the
subjects was from 21 to 40 yr (mean age 29 yr). Thirteen
male subjects and 15 female subjects were enrolled. Each
participant completed spirometric testing that included
forced vital capacity and forced expiratory volume in 1 s. The
forced expiratory volume in 1 s-to-forced vital capacity ratio
was 70% for each participant. Subjects had no history of
oropharyngeal dysphagia or complaints about oropharyngeal
swallowing function. Participants recruited were free of ac-
tive upper respiratory infection at the time of data collection.
Data Acquisition
Swallows were recorded by using simultaneous videofluo-
roscopy for timing measurements, bipolar intramuscular
J Appl Physiol VOL 95 DECEMBER 2003
electromyography (EMG) of pharyngeal muscle activity, and
a respiratory inductance plethysmograph (Respitrace, Ambu-
latory Monitoring, Ardsley, NY) to record respiratory phases
and estimated lung volumes. WinDaq waveform recording
software (DATAQ Instruments, Akron, OH) was used to
collect, organize, and analyze the EMG and respiratory data.
The Kay swallowing workstation (Kay Elemetrics, Lincoln
Park, NJ) was used to record and analyze the fluoroscopic
data. All data were collected during a single session lasting
1 h.
EMG Instrumentation
Before data collection, bilateral intramuscular EMG elec-
trodes were placed in the lower, lateral margin of the supe-
rior pharyngeal constrictor, according to the method de-
scribed by Perlman et al. (32). EMG signals were preampli-
fied and filtered (Grass Instruments, Astro-Med, West
Warwick, RI). The EMG and the output of the Respitrace
were routed through anti-aliasing filters (RC Electronics,
Santa Barbara, CA). The signals were digitized with WinDaq
software (DATAQ Instruments).
Respiratory Instrumentation
The Respitrace (Respitrace, Ambulatory Monitoring) is a
respiratory inductance plethysmograph composed of two
elasticized cloth bands with Teflon-insulated wire coils at-
tached within. One band is placed around the rib cage under
the arms, and the other band is placed around the waist.
Each band measures the changes in the cross-sectional area
of the rib cage and abdomen, allowing for the determination
of changes in lung volume and monitoring of respiration
phase. Unlike other methods of measuring ventilation, the
Respitrace does not require any apparatus involving the face,
making it ideal for a deglutition study.
Reliable calibration of the Respitrace was not possible
during this study because of the extremes in lung volume
that were randomly required throughout each individual
data collection session (26, 35). The signal from the Respi-
trace was used to provide visual feedback to assist the par-
ticipants in controlling their lung volumes and as visual
assurance during data analysis that each participant
achieved the target lung volumes in response to the verbal
directions.
Videoradiographic Instrumentation
Videofluoroscopy was used to record swallowing physiol-
ogy and bolus transit through the pharynx. The superior
margin of the image was set consistently to contain the
nasopharynx. The anterior fluoroscopic view was set to in-
clude the anterior tongue and alveolar ridges. The posterior
margin of the image included the cervical bodies. Lastly, the
inferior margin was set to include the upper one-third por-
tion of the trachea. The inclusion of all of these areas ensured
direct observation of entire oropharyngeal swallow. The im-
age was magnified 2 to increase the detail of each subjects
anatomy. The Kay swallowing workstation recorded all flu-
oroscopic data and audio data.
Data Acquisition Protocol
Considering that Psub during the swallow cannot be mea-
sured noninvasively in nontracheotomized participants, the
polarity of Psub was inferred by having participants swallow
at total lung capacity (TLC), which is consistent with the end
of maximal inhalation and before the onset of exhalation
(highest positive Psub), at resting expiratory level or func-
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 LUNG VOLUME EFFECTS ON SWALLOWING
tional residual capacity (FRC), where recoil forces are inac-
tive or less active (34% vital capacity equating to a lower or
midrange Psub), and at residual volume (RV), which is the
end of forced exhalation and before the onset of inhalation
(0% vital capacity and lowest Psub or negative). Partici-
pants were observed swallowing three separate, standard-
ized 5-ml pudding-consistency barium boluses under video-
fluoroscopy, with simultaneous recordings of pharyngeal
EMG and Respitrace output at each of the three targeted
lung volumes. The pudding boluses were taken from a mix-
ture of 30 ml of Intropaste barium sulfate paste (Lafayette
Pharmaceuticals, Lafayette, IN) and 60 ml of pudding (Hunts
snack pack, Hunt-Wesson, Fullerton, CA). The resulting mix-
ture had a viscosity of 5,800 cP. The viscosity of the pud-
ding and barium mixture was measured by using a Brook-
field DV-I Viscometer at ambient temperature (spindle no.
4 at 20 rpm). A syringe was used to measure the 5-ml bolus
onto the spoon. In all cases, the pudding bolus was placed in
the subjects mouth with a teaspoon. The three conditions
were randomized within and between subjects to avoid order
effects and/or habituation to any of the lung conditions.
Three swallows at each lung volume were recorded for a total
of nine swallows per subject.
EMG Data Analysis
Out of 252 total swallows recorded, 48 were removed from
final analysis because they did not occur at the targeted lung
volume. The complete data sets of two subjects were removed
entirely because of poor respiratory data. Respiratory data
were judged as inadequate for analysis when the deflection of
the signal was not large enough to allow for confident deter-
mination that the target lung volumes had been obtained.
The inadequate signal was most likely the result of too
loosely placed bands. Although every attempt was made to
place and maintain two electrodes in each subject, only one
channel of EMG could be analyzed per subject. Out of 204
remaining swallows, 49 swallows could not be analyzed be-
cause of electrode dislodgment. Electrode dislodgment was
most likely attributable to the combined motion of swallow-
ing and the high viscosity of the bolus. Furthermore, after
review of the videofluoroscopic tapes, six more swallows were
removed because it was discovered that the subject had split
the bolus in two rather than swallow the entire bolus in one
swallow. Therefore, a total of 149 swallows (or 14 subjects
with complete data sets) were entered into the final EMG
analysis.
Physiological Measurements Taken From EMG
WinDaq interactive software (DATAQ Instruments) was
used to analyze the duration and amplitude of the superior
pharyngeal constrictor EMG signal during the swallow. The
signal was rectified, digitized, and integrated over time. For
each swallow, the duration of the signal was determined by
selecting the onset and offset of the rectified signal. Once the
signal duration was established, the signal amplitude was
determined by calculating the mean rectified and integrated
EMG over a fixed interval of 800 ms (23). The value 800 ms
was selected before data analysis because this is the mean
swallow duration reported by Perlman et al. (32). The aver-
age of the three swallows per condition was used for final
analysis.
Fluoroscopy Data Analysis
Out of 204 swallows, 179 individual swallows (22 subjects
with complete data sets) were used for the final fluoroscopic
J Appl Physiol VOL 95 DECEMBER 2003
2213
analysis. A total of 25 swallows were removed from the
fluoroscopic analysis because the bolus was split into two
swallows, the fluoroscope was turned on late, the contrast of
the X-ray was too dark to see pertinent anatomy, or the
subject moved during the swallow. Swallows of poor EMG
quality, but occurring at the target lung volume, were not
excluded from the fluoroscopic analysis.
Physiological Measurements Taken From Videofluoroscopy
Bolus transit time. The starting point for bolus transit time
(BTT) was taken from the first videofluoroscopic frame,
where the head of the primary bolus reaches the lower
margin of the mandible. The primary bolus was defined as
the portion of the bolus being actively propelled by the
tongue. The end point was taken when the superior margin of
the cricopharyngeal sphincter was observed to close behind
the tail of the primary bolus. BTT was measured three
times for each swallow, and the average value was used for
analysis.
Pharyngeal activity duration. Pharyngeal activity dura-
tion (PAD) is a measurement that was established for the
purpose of distinguishing the pharyngeal motor response
time from BTT. PAD also distinguishes between hyoid mo-
tion onset associated with the phase transition time period
(between the oral and pharyngeal phases) and the anterior
hyoid thrust that is associated primarily with the onset of the
pharyngeal swallow.
The starting point was the first frame in which the onset of
hyoid motion associated with the pharyngeal swallow was
observed. The ending point was taken as the first frame in
which air was again observed in any portion of the pharynx.
PAD was also measured three times for each swallow, and
the average value was used for analysis.
Aspiration-penetration severity level. Assignment of the
aspiration-penetration score (34) was made after three obser-
vations of each swallow.
RESULTS
To determine redundancy of the dependent vari-
ables, correlations between the dependent measures
were calculated by using the one-tailed Pearson corre-
lation with a significance level set at 0.01. EMG dura-
tion showed a significant correlation of 0.68 and 0.76
for BTT and PAD at TLC (P 0.007 and 0.00138,
respectively). The correlation coefficient of 0.767 met
the predetermined criterion of 0.80 for removal; how-
ever, this finding occurred in only one combination at
one level of the independent variable. Therefore, none
of the variables was removed from the final analysis.
Penetration and Aspiration Scores
No aspiration or penetration was observed on any
swallow for any lung volume. All swallows were rated
1 (no aspiration or penetration within the laryngeal
vestibule).
Statistical Analyses
The means, SDs, and SEs are displayed for each
dependent variable in Table 1. Normality testing (Kol-
mogorov-Smirnov) showed that EMG amplitude, EMG
duration, and BTTs were normally distributed. A sin-
gle-factor repeated-measures analysis of variance was
performed for each measure, utilizing respiratory vol-
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2214 LUNG VOLUME EFFECTS ON SWALLOWING

Table 1. Mean, SD, SE, and number of subjects for Table 3. Student-Newman-Keuls
the three lung conditions (TLC, FRC, RV)
Comparison Difference in Ranks q P 0.05
Mean SD SE n
PAD-RV vs. PAD-FRC 16.000 3.411 Yes
EMG amplitude, mV PAD-RV vs. PAD-TLC 14.000 4.221 Yes
PAD-TLC vs. PAD-FRC 2.00 0.603 No
TLC 5.37 4.36 1.17 14
FRC 5.30 4.03 1.08 14 PAD, pharyngeal activity duration.
RV 5.11 4.00 1.07 14
EMG duration, ms
high at 93% agreement. Intrarater and interrater reli-
TLC 952.00 118.00 31.50 14
FRC 902.00 166.00 44.50 14 ability were measured for EMG duration and ampli-
RV 1,000.00 126.00 33.70 14 tude by reanalyzing 30 randomly selected swallows
Bolus transit time, ms representing 20% of the total 149 swallows that went
on to final data analysis. Intrarater reliability was high
TLC 521.00 81.40 17.40 22
FRC 527.20 55.70 11.90 22 at 0.815 for EMG duration and 0.999 for EMG ampli-
RV 520.00 72.40 15.40 22 tude. Interrater reliability for EMG duration was 0.714
Pharyngeal activity duration, ms and 0.737 for amplitude. To determine the intra- and
interrater reliability for the fluoroscopy measurements
TLC 690.00 112.00 24.00 22
FRC 694.00 122.00 26.00 22 BTT and PAD, 20% of the total 179 swallows, or 35
RV 719.50 105.00 22.30 22 swallows, were randomly selected and remeasured.
Intrarater reliability was high at 0.844 for BTT and
n, No. of subjects. EMG, electromyography; TLC, total lung capac-
ity; FRC, functional residual capacity; RV, residual volume.
0.846 for PAD. Interrater reliability for BTT was high
at 0.790 for PAD but was moderate at 0.640 for BTT.
Intra- and interrater reliability on the penetration and
ume as the within-group factor. Significant differences aspiration scale were both 100%.
between the means were not found. Table 2 displays
DISCUSSION
the calculated values.
Motivated by the notion that the anatomic overlap of
PAD
the respiratory and alimentary tracts along with the
The PAD data were not normally distributed (P intermingling of brain stem neurons involved in respi-
0.006) and were subsequently analyzed by using the ration and swallowing enable processing of sensory
Friedman repeated-measures analysis of variance. The information across systems, we hypothesized that al-
differences in the median values at the different levels terations in the respiratory system could elicit physio-
of the independent variable were found to differ signif- logical changes in pharyngeal swallowing function.
icantly (P 0.032). The Student-Newman-Keuls pair- This hypothesis was based on the subglottic pressure
wise multiple comparison procedure revealed that theory and the findings of several experiments in
PAD-RV was significantly longer in duration than which aspiration was reduced or eliminated in subjects
PAD-TLC and PAD-FRC. Table 3 displays the results with indwelling tracheostomy tubes when the tube was
of the post hoc analysis. closed, allowing for the buildup of Psub during the
swallow (11, 27, 43). Consistent with the theory that
Reliability Psub may be integral to efficient swallowing, statistical
Several reliability measures were computed. To as- analysis of the data revealed a significantly longer
certain the intrarater reliability for the determination duration of PAD for swallows that occurred in the low
of acceptable lung volume at the time of the swallow, subglottic pressure condition (RV) compared with
50 swallow and breath combinations, representing 20% swallows that occurred at higher lung volumes (TLC
of the total number of swallows (252), were randomly and FRC). Convergent validity is provided in previous
selected. The 50 swallow and breath combinations work by Logemann et al. (22) and Gross et al. (16) in
were then reanalyzed (acceptable vs. not acceptable). which longer contraction times of pharyngeal swallow-
The percent agreement was high at 88%. Intrarater ing musculature were measured when tracheostomy
reliability for the selection of EMG data was also com- tubes were open (zero Psub) compared with closed
pleted on 30 randomly selected swallows and was also tubes in which Psub during the swallow could be gen-
erated.
Gross et al. (16) found that, in tracheostomy sub-
Table 2. Repeated-measures ANOVA jects, PAD duration could increase as much as 314 ms
when the tube was opened and subglottic air pressure
Variable SS df MS f P was zero. They postulated that a feed-forward system
Amp EMG 0.0005 2 0.0003 0.171 0.844 may detect the loss of Psub and that the timing differ-
Duration EMG 67.4 2 33.7 2.60 0.094 ence was long enough to allow for cortical processing.
BTT 778.5 2 389.3 0.328 0.722 In this experiment, the largest timing difference in
BTT, bolus transit time; SS, sum of squares; df, degrees of freedom; PAD was 32 ms and occurred between TLC and RV at
MS, mean squares. 32 ms. This small durational difference also rules out
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 LUNG VOLUME EFFECTS ON SWALLOWING
the possibility of a closed-loop feedback controller and
lends support for feed-forward (predictive) modulation
(1, 14, 36). How subglottic mechanoreceptors may con-
trol and alter swallowing function in a closed system
(no indwelling tracheostomy tube) where Psub is a
function of lung volume, as well as the significance of
the durational differences measured in this experi-
ment, can be further discussed and interpreted via the
theoretical framework of motor control.
Motor Planning Theory
Open-loop theory, developed as a linear paradigm to
understand ballistic movement (2.5), eventually es-
corted in the search for neural substrates such as the
central pattern generator (CPG) (14). This paradigm
states that information processing or preplanning (top
down) occurs before the movement is executed.
Schmidt (36) altered the model such that the stored
program was general rather than specific. A general
motor program would, therefore, permit adjustments
to be incorporated into the preplanning stage (prescrip-
tive approach) as a means of improving or ensuring
accuracy of the movement. Feed-forward controllers
operate most precisely in a context in which experi-
ence-based motions are executed. Significant positive
correlations between EMG duration, BTT, and PAD
were present only for swallows occurring at TLC. If
TLC most closely approximates the initiation of the
most efficient motor program, then these correlations
may be indicative of the condition that is closest to the
swallowing program (i.e., the lungs are filled and Psub
is likely to be sufficiently positive).
PAD of swallows occurring at FRC were not signifi-
cantly different from TLC, perhaps because the poten-
tial to generate positive pressure was still present.
PAD-FRC was significantly shorter than PAD-RV,
with a median difference of 17 ms. Interesting, these
midlung range swallows were nearly one-half the time
duration difference between TLC and RV (Fig. 1). The
meaning of this relationship, if any, is unclear; how-
Fig. 1. Pharyngeal activity duration (PAD). Median, 25th, and 75th
quartiles are shown. TLC, total lung capacity; FRC, functional re-
sidual capacity; RV, residual volume.
J Appl Physiol VOL
2215
ever, it may further suggest the possibility of a linear
relationship (consistent with the predictive model) be-
tween lung volume and PAD should a range of lung
volumes be studied in the future. Conceivably, a target
lung volume range for optimal swallowing function
may exist.
Perhaps the status of the respiratory system at the
time when swallow elicitation was required to occur
within this protocol (especially at RV) presented a
potential disturbance. When a disturbance is de-
tected, neural swallowing components may calculate
the effects that the disturbance was likely to have on
the swallow and respond by enabling functions re-
quired to counteract these effects (18). Again, it is
possible that the condition of the respiratory system
before the swallow resulted in an altered or corrected
durational parameter descending from the suprabul-
bar structures and onto the CPG, thereby ensuring the
success of the swallow (i.e., avoidance of aspiration).
Another possibility is that the adjustments to PAD
did not occur before the onset of the motion pattern. If
the swallow is viewed as a single act occurring within
the context of different levels of Psub, then a pertur-
bation may have occurred when the true vocal folds
closed and a change in Psub was detected. Perchance
the increased duration in the RV condition is indicative
of the swallow being reprogrammed intramovement
at the level of the CPG to minimize or avoid the
possible detrimental influence of swallowing without
sufficient Psub (36).
Dynamic Systems Theory
Another explanation for motor control is the action
systems approach, also known as the dynamic sys-
tems theory. The dynamic paradigm is a nonlinear
model intended to encompass all levels of motion, from
the psychological to neural substrates. Action and per-
ception are tightly coupled with motor control and
executed in a bottom-up fashion through the employ-
ment of coordinative structures, as opposed to the
top-down control model represented by open-loop the-
ory (2, 7, 37). Such coordinative structures operate
within environmentally controlled constraints that ul-
timately impact the number of degrees of freedom
available for movement pattern execution. The dy-
namic system seeks the condition of highest equilib-
rium known as an attractor state (47). The findings
from this study can also be explained by the dynamic
paradigm, if one would consider swallowing at higher
lung volumes and positive Psub (FRC and TLC) to be
viewed as attractor states.
Based on the results of this experiment that show an
influence of the respiratory system on swallowing, the
larynx and pharynx, along with their neural sub-
strates, may serve as coordinative structures. In the
dynamic model, the mechanoreceptors of the subglottic
larynx may have induced a new, unestablished attrac-
tor state, or applied a constraint on the swallowing
structures, when low Psub (RV) was revealed during
the swallow as the true vocal fold adducted. To ensure
95 DECEMBER 2003 www.jap.org
2216 LUNG VOLUME EFFECTS ON SWALLOWING
the successful completion of the overall motion goal
(i.e., swallowing without aspiration), the coordinative
structures changed their synergistic motions via com-
pensatory adjustments that prolonged PAD (20). The
temporal changes that occurred during pharyngeal ac-
tivity at the different lung volumes may yet be further
explained by the direct application of dynamic theory
to the CPG for swallowing.
Dynamic Theory and CPGs
Conceivably, dynamic systems theory can be used as
a heuristic device for explaining the prolonged dura-
tion of PAD at RV compared with TLC and FRC. The
durational difference between the conditions may be
indicative of the underlying neural mechanisms within
the brain stem CPGs for respiration and swallowing,
wherein the neuronal network was forced to select
alternative neural connections when signaled by the
larynx as to the condition (pressure) of the airway
during the swallowing sequence. A model that ad-
dresses such a concept has been proposed by Chiel et
al. (10).
Chiel et al. (10) developed a quantitative model of
the dynamics of CPGs in walking in an attempt to
provide quantitative insight into their operation. They
theorized that neural circuits might be dynamically
reconfigured by intrinsic and extrinsic neuromodula-
tion. The authors envisioned the CPG as possessing a
steady state (attractor state), where it functions op-
timally with highest speed and efficiency. Whereas
these authors performed complex mathematics using a
three-neuron model for walking, several of the analo-
gies they described can be used to help to understand a
possible explanation for the increased duration of the
PAD in the RV condition. Because swallowing is cur-
rently believed to be governed by a CPG, as is walking,
it is not unreasonable to make comparisons between
gait and swallowing at the level of the CPG.
Time constraints within a CPG originate from the
relationships of their synaptic connections to one an-
other. Variations exist in the strength of both inhibi-
tory and excitatory connections between all neuronal
components. Steady-state function within a CPG
would most likely have the strongest of both types of
synaptic connectivity. Within the steady-state condi-
tion, the rate of change of the output would be zero.
Neural circuits can be phasically altered by sensory
feedback that can transiently inject synaptic currents
into different neurons more loosely bound to the
steady-state group. This condition would result in the
need for the CPG to make a transition away from the
steady state by using alternative connections and neu-
rons. A new set of constraints would then exist and be
dependent on the duration of the transition and the
sensitivity or robustness of the briefly reconfigured
module. Mathematically, if, for example, five transi-
tions were required, the sum of their durations would
then equal the total duration of the resulting motor
pattern. Therefore, increased durations would be mea-
sured in motor patterns or sequences that occur away
J Appl Physiol VOL
from the steady-state function compared with the
steady state.
Applying this logic to our experiment, swallowing at
TLC or FRC may be at the steady-state condition or
nearest to the actual attractor state for swallowing.
Swallowing at RV, however, may have prompted the
need for several transitions within the CPG in order for
successful swallowing to occur. As was previously
stated, the number of transitions and robustness of the
synaptic currents, when summed, would equal the to-
tal duration of the motor pattern. Therefore, the PAD
was significantly longer when swallows occurred at RV
(lowest entropy/furthest away from steady-state or at-
tractor state) compared with swallows occurring at
both TLC and RV.
In summary, swallowing is an essential motor pat-
tern that incorporates peripheral sensory information
into its motor output. There is now a strong implica-
tion, based on this experiment and others, that a por-
tion of the afferent information may come from the
respiratory system. This determination would dispel
the current conception of the interaction between res-
piration and swallowing as a simple reciprocity and
expand the understanding to that of an interactive
cooperation.
The value of continued exploration into this matter
could ultimately benefit individuals who suffer from
neurological insults, such as stroke or Parkinsons dis-
ease. For example, in patients with stroke, prolonged
pharyngeal transit times have been identified as one of
the risk factors for developing aspiration pneumonia
(17). Furthermore, it has been suggested that persons
with neurological impairment may show a disorgani-
zation of the normal coordination of respiration and
swallowing and may swallow at points in the respira-
tory cycle when lung volumes (and subsequently Psub)
are low (39). Perchance the omission of respiratory
information in the diagnosis and treatment of dyspha-
gia in todays clinical practice may reduce diagnostic
accuracy and treatment effectiveness if normal respi-
ratory patterning during deglutition is critical to safe
swallowing. Ultimately, the development of treatment
paradigms for oropharyngeal dysphagia may take re-
spiratory status into consideration.
Future experiments that seek to measure swallow-
ing muscle activity and respiratory measures may re-
duce data loss by employing submental EMG measure-
ments that will not be subject to dislodgment from
bolus passage or by using a bipolar suction electrode
(30). To minimize respiratory data loss, subjects could
be briefly trained before data collection with the Respi-
bands in place; however, this could pose a threat to
internal validity, because habituation may take place
before data collection.
We are grateful to Drs. Malcolm R. McNeil, Jessie M. Van Swear-
ingen, and Patrick J. Doyle for technical and editorial guidance.
DISCLOSURES
This study was supported by the Veterans Affairs Geriatric Re-
search Education and Clinical Center.
95 DECEMBER 2003 www.jap.org
 LUNG VOLUME EFFECTS ON SWALLOWING
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