Content uploaded by Wolbert van den Hoorn
Author content
All content in this area was uploaded by Wolbert van den Hoorn on May 12, 2016
Content may be subject to copyright.
Available via license: CC BY 4.0
Content may be subject to copyright.
RESEARCH ARTICLE
Breathing and Singing: Objective
Characterization of Breathing Patterns in
Classical Singers
Sauro Salomoni, Wolbert van den Hoorn, Paul Hodges*
The University of Queensland, Centre for Clinical Research Excellence in Spinal Pain, Injury and Health,
School of Health and Rehabilitation Sciences, Brisbane, Australia
*p.hodges@uq.edu.au
Abstract
Singing involves distinct respiratory kinematics (i.e. movements of rib cage and abdomen)
to quiet breathing because of different demands on the respiratory system. Professional
classical singers often advocate for the advantages of an active control of the abdomen on
singing performance. This is presumed to prevent shortening of the diaphragm, elevate the
rib cage, and thus promote efficient generation of subglottal pressure during phonation.
However, few studies have investigated these patterns quantitatively and inter-subject vari-
ability has hindered the identification of stereotypical patterns of respiratory kinematics.
Here, seven professional classical singers and four untrained individuals were assessed
during quiet breathing, and when singing both a standard song and a piece of choice. Sev-
eral parameters were extracted from respiratory kinematics and airflow, and principal com-
ponent analysis was used to identify typical patterns of respiratory kinematics. No group
differences were observed during quiet breathing. During singing, both groups adapted to
rhythmical constraints with decreased time of inspiration and increased peak airflow. In con-
trast to untrained individuals, classical singers used greater percentage of abdominal contri-
bution to lung volume during singing and greater asynchrony between movements of rib
cage and abdomen. Classical singers substantially altered the coordination of rib cage and
abdomen during singing from that used for quiet breathing. Despite variations between par-
ticipants, principal component analysis revealed consistent pre-phonatory inward move-
ments of the abdominal wall during singing. This contrasted with untrained individuals, who
demonstrated synchronous respiratory movements during all tasks. The inward abdominal
movements observed in classical singers elevates intra-abdominal pressure and may
increase the length and the pressure-generating capacity of rib cage expiratory muscles for
potential improvements in voice quality.
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 1/18
a11111
OPEN ACCESS
Citation: Salomoni S, van den Hoorn W, Hodges P
(2016) Breathing and Singing: Objective
Characterization of Breathing Patterns in Classical
Singers. PLoS ONE 11(5): e0155084. doi:10.1371/
journal.pone.0155084
Editor: Charles R Larson, Northwestern University,
UNITED STATES
Received: January 31, 2016
Accepted: April 23, 2016
Published: May 9, 2016
Copyright: © 2016 Salomoni et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are
credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information files.
Funding: PH was supported by a Senior Principal
Research Fellowship (ID1002190) from the National
Health and Medical Research Council (NHMRC) of
Australia. The study was supported by a Centre of
Clinical Research Excellence Grant (ID455863) and
Program Grant (ID631717) from the NHMRC. The
funders had no role in study design, data collection
and analysis, decision to publish, or preparation of
the manuscript.
Introduction
Breathing patterns during speaking and singing can differ from that during quiet breathing by
modification of respiratory kinematics (i.e. movements of rib cage and abdomen) in response
to altered task demands. Active control of breathing pattern affects the efficiency of the respira-
tory system and is considered essential in classical singing training for the development of opti-
mal voice performance [1–4]. Experienced singers and teachers commonly refer to the use of
abdominal muscle “support”to improve respiratory control and tone quality [4–7]. Although
an agreed definition of the term “support”remains elusive [8,9], it is generally considered to
involve enhanced abdominal muscle activation, which elevates intra-abdominal pressure and
expands the rib cage, thus increasing the length and the pressure-generating capacity of the rib
cage expiratory muscles [10]. However, attempts to identify stereotypical patterns of respira-
tory kinematics in classically trained singers have been so far inconclusive [2,6,11,12], and it is
unclear how the breathing pattern of classical singers differ from that of untrained individuals.
According to the National Association of Teachers of Singing, focus on abdominal breath-
ing is one of the most effective directives when teaching breathing support [9,13]. Although the
specific role of individual muscles during phonation remains debated [10,14–20], greater acti-
vation of abdominal muscles is generally observed during speaking and singing than quiet
breathing [16,17]. From visual inspection of respiratory kinematics, it has been suggested that,
during singing, classical singers contract abdominal muscles at the end of the inspiration
phase, which is argued to produce pre-phonatory inward movement of the abdomen [2,12].
This would summate with the passive recoil characteristics of chest wall and lungs in prepara-
tion for efficient generation of expiratory airflow [4,21–23]. During phonation, contracted
abdominal muscles prevent shortening of the diaphragm [17] and provides the opposing force
required for the rib cage to develop strong subglottal pressure in order to increase sound pitch
and/or loudness [2,6,15,24]. Furthermore, the elevated position of the ribs increases rib cage
volume and allows for quick phonatory manoeuvres [25,26]. The independent and asynchro-
nous movements between the rib cage and abdominal wall often results in paradoxical motion,
characterized by compartmental volume displacement opposite in sign to lung volume change,
such as increased volume of the rib cage during expiration/phonation phase of the breath cycle
[2].
Previous studies have assessed classical singers during singing performances with and with-
out use of the supported voice strategy [4,6,20,27]. The results suggest that the supported voice
is associated with greater subglottal pressure, greater sound pressure, and higher peak airflow.
Together, this leads to a requirement for larger air volumes to produce the same musical
phrases and has been suggested to influence high frequency bands of the sound power spec-
trum [6,28]. However, two issues hinder the generalization of these findings. First, considerable
inter-subject variability has been reported in most studies [6,29]. Second, although professional
classical singers often repeat consistent patterns of respiratory kinematics when repeating the
same musical task [30,31], when they are asked to perform with an “unsupported”voice, they
must artificially emulate a non-habitual (and otherwise never used) breathing pattern, and it is
unclear whether it is possible to avoid features of their own habitual patterns [7,32].
Studies that compare group averages of data recorded from classical singers with previous
observations from untrained individuals [33] have suggested that professional singers initiate
musical phrases at higher lung volumes [3], although conclusive statistical tests have not
been performed. Moreover, classical singers showed greater deformation of the rib cage and
abdominal wall in respiratory adjustments during singing than during speaking tasks [2,12],
whereas untrained individuals and professional country singers used similar strategies during
both tasks [33,34]. However, these observations have been based on qualitative/subjective
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 2/18
Competing Interests: The authors have declared
that no competing interests exist.
assessments, often relying on visual inspection of raw data, thus providing limited support to
infer about typical patterns of respiratory kinematics of classically trained singers. In order to
identify the unique features of the breathing patterns of classical singers, it is necessary to
perform direct and objective comparison between professional singers and untrained
individuals.
The aim of the current study was to objectively characterize dynamic patterns of respiratory
kinematics during quiet breathing and singing in order to: (i) compare the features of breathing
patterns of professional classical singers with a group of untrained individuals during a stan-
dardised singing task; and (ii) investigate whether breathing patterns differed between quiet
breathing and singing for each group. We hypothesized that, in contrast to untrained individu-
als, classically trained singers would demonstrate: (i) greater contribution of abdominal volume
to total lung volume; (ii) weaker correlation between movements of the rib cage and the
abdominal wall when singing; and (iii) this would reflect greater asynchrony between move-
ments of the rib cage and abdomen during singing than quiet breathing. Finally, (iv) higher
inter-subject variability is expected among professional singers than untrained controls due to
the development of subject-specific techniques of respiratory kinematics.
Methods
Participants
Seven professional classical singers (two males, aged from 39 to 41; five females, aged from 24
to 72) and four untrained individuals (control group, all males, aged from 21 to 41) partici-
pated in this study. Table 1 presents demographic data and information about singing training
and performing experience from participants (anthropometric information for classical singer
#3 is not available). All participants were native English speakers, and provided written
informed consent prior to inclusion. The Medical Research Ethics Committee of The Univer-
sity of Queensland approved the study, which was conducted in accordance with the Declara-
tion of Helsinki.
Table 1. Anthropometric parameters and information about formal training and performing experience from classical singers and untrained indi-
viduals (controls).
Classical Control
#1 #2 #3 #4 #5 #6 #7 #1 #2 #3 #4
Age (yrs) 61 27 29 41 72 24 39 37 21 36 41
Gender FFFMF FMMMMM
Height (cm) 165 160 N/A 178 165 172 182 184 175 173 182
Weight (kg) 60 61 N/A 75 56 82 86 84 65 64 69
BMI (kg/m2) 22.0 23.8 N/A 23.6 20.5 27.7 25.9 24.8 21.2 21.3 20.8
Training experience (yrs) 7 5 10 8 20+ 6 10 - - - -
Performing experience (yrs) 35 8 10 21 30+ 6 20 - - - -
Full- or Part-time Singer Part-time Part-time Full-time Full-time Full-time *Full-time Full-time - - - -
Solo or Choral Singer Both Choral Solo Solo Both Solo Solo - - - -
Recital or Opera Singer Recital - Opera Opera Both Both Opera - - - -
Notes: Anthropometric parameters not available (N/A) for classical singer #3.
*Classical singer #5 currently works primarily as a singing teacher.
F: Female.
M: Male.
doi:10.1371/journal.pone.0155084.t001
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 3/18
Inductance plethysmography
Respiratory kinematics were estimated using respiratory inductance plethysmography bands
(Inductotrace, Ambulatory Monitoring Inc., USA). One band was placed around the rib cage
with the upper edge below the axilla, and the other placed around the abdomen, between the
lowest rib and the iliac crest. In order to minimize potential effects of temperature-related base-
line drift in the signal, a warm up period of 15–30 minutes was allowed after placing the elastic
bands. Moreover, volume parameters were calculated within individual breath cycles, during
which the baseline drift was negligible.
Airflow
Airflow was recorded using a pneumotachograph (Hans Rudolf Inc., USA) connected to a dif-
ferential pressure transducer (Validyne Engineering, USA). Phonation was recorded using a
headset microphone (Allans Billy Hyde, Australia), and was used to assist identification of
event timings in the respiratory data. All analogue signals were A/D converted and recorded at
2 kHz using a CED1401 data acquisition system and Spike2 software (Cambridge Electronic
Design, UK).
Experimental procedure
Data acquisition started with the calibration of the pneumotachograph using a 3000 mL preci-
sion syringe (Hans Rudolph Inc., USA). Participants then performed an isovolume manoeuvre,
which consisted of alternate expansion of the rib cage and abdomen with the glottis closed, for
estimation of the total lung volume as the weighted sum of rib cage and abdominal compart-
mental volumes [35]. Following the calibration procedures, each participant performed the fol-
lowing tasks in standing position:
1. Quiet breathing for 1 minute;
2. Singing the traditional Australian song Waltzing Matilda, which was well known to all par-
ticipants. Classical singers sang this song in operatic style, whereas control participants sang
in the traditional folk style;
3. Singing a piece of the participant’s choice (1–2 minutes), which for the classical singers
involved an operatic piece. This task was chosen to observe respiratory kinematics when
subjects performed a song with which they were familiar and allowed classical singers to
demonstrate their usual singing technique.
Tasks 2 and 3 were repeated twice, and were performed without instrumental accompani-
ment (i.e. “a capella”). The first repetition was completed without a facemask, whereas in the
second participants sang wearing a pneumotachograph facemask over the mouth and nose. An
experimenter stood next to the participant to support the weight of the facemask, such that
participants could maintain the same body posture during both repetitions without additional
load to the head and neck, which could have influenced their breathing patterns.
Data analysis
Rib cage (RC) and abdominal wall (AB) plethysmographic signals were calibrated using the
weightings derived from the isovolume manoeuvre and the volume changes measured with the
pneumotachograph. Total lung volume was estimated as the weighted summation of RC and
AB signals. Data were low-pass filtered at 10 Hz (second-order Butterworth filter) to remove
high-frequency instrumentation noise. Individual breath cycles (inspiration and expiration
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 4/18
phases) were identified from local maxima and minima lung volume, with reference to the air-
flow (when available) and audio signals to aid the identification process. Inspiration phase was
identified as the periods of negative airflow, with a transition from minimal to maximal lung
volume. Similarly, expiration/phonation phase was identified as the period from maximal to
minimal lung volume, with positive airflow and activity of the audio signal. Although some
studies have identified phonation phase solely based on audio events [31], this procedure
ignores the transition between inspiration and expiration/phonation phases, which is of partic-
ular interest in the characterization of breathing patterns.
The following parameters were extracted from the RC and AB volume signals and averaged
over all breath cycles for each participant: Respiratory frequency (Fres, breaths/minute), time
of inspiration (Ti, seconds), and percentage of rib cage contribution to total lung volume (%
RC) (Fig 1).
The association between movements of the RC and AB was assessed using different parame-
ters. The similarity between RC and AB was measured using the Pearson coefficient of linear
correlation (r), averaged across all individual breath cycles. The amount of asynchrony between
volume compartments was estimated by maximal cross-correlation [1] and expressed as phase
angle. In order to investigate the transition between inspiratory and expiratory phases, the time
shift between the moments of maximal volume of RC and AB was estimated (Fig 1). Consistent
with the interpretation of the phase angle, a positive time shift was defined as a peak in AB vol-
ume occurring before that in RC volume. The duration of paradoxical motion of each volume
compartment during expiration/phonation phase (i.e. paradoxical expansion of the RC or AB,
reflecting asynchrony in respiratory kinematics) was quantified during each breath cycle and
expressed as percentage of breath cycle length. The corresponding air volume moved during
the period of paradoxical motion was expressed as percentage of total expiratory volume.
Theairflowsignalfromthepneumotachograph was calibrated against the high-precision
syringe using a third order polynomial fit procedure [5], and corrected to account for the differ-
ence in dynamic viscosity between inspired and expired gases in BTPS (body temperature and
pressure, saturated with water vapour) and ambient conditions. The corresponding respiratory
volume was estimated by numerical integration of the differential airflow signal. The calibrated air-
flow and volume signals were then used to assess peak airflow, mean airflow, and volume excur-
sion during expiration/phonation phase (i.e., the difference between the volume at phase initiation
and termination). Airflow data was not recorded for one classical singer for technical reasons.
Fig 1. Illustration of rib cage (RC), abdominal (AB) and total lung volumes during three breath cycles of a classical singer performing a
singing task (task 1: Waltzing Matilda). Parameters assessed from respiratory waveforms are indicated: respiratory frequency (Fres), time of
inspiration (Ti), RC volume and time shift between peak volume of RC and AB.
doi:10.1371/journal.pone.0155084.g001
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 5/18
Finally, in order to objectively characterize the typical breathing patterns of classical singers
and untrained individuals, Principal Component Analysis (PCA) was performed on RC and
AB volume signals (Fig 2A). Briefly, PCA is a mathematical procedure used to identify com-
mon patterns from large sets of input signals [8]. In the current study, the volume signals from
all breath cycles were used as input signals for the PCA to generate a reduced new set of signals,
called Principal Components, reflecting the most common features of the input data set. Each
input signal was then represented as a weighted sum of a small number of Principal Compo-
nents, where the weights are called PCA coefficients (Fig 2B). Usually in human movement
analysis, the first Principal Component alone is able to explain more than 50% of the variability
of all input signals, and the inclusion of additional Components gradually improves the accu-
racy of the PCA representation [11]. In the current study, the number of Principal Compo-
nents was determined using a scree test, retaining all components with eigenvalues greater
than 0.5% of the total variance (Fig 2C). As the length of the breath cycles were not identical,
volume signals were time-normalized to 1,000 data points and expressed as a percentage of
cycle length [13]. The amplitude of RC and AB volume signals was normalized in relation to
the maximal lung volume of the corresponding breath cycle, therefore retaining the relative
contribution of each compartment. Moreover, this method of amplitude normalization also
compensates for differences in lung volume across multiple breath cycles. Classical singers and
Fig 2. Example of extraction of typical breathing patterns using Principal Component Analysis (PCA). In A, rib cage (RC) and
abdominal (AB) volumes are shown for three consecutive breath cycles of a classical singer performinga singing task (task 1: Waltzing
Matilda). These waveforms were used to calculate the PCA components and PCA coefficients shown in B. In this example, three
components explained more than 98% of the total variability of the original signals. The PCA representations in C were obtained by
weighting the PCA components by the corresponding PCA coefficients. The typical breathing pattern for this subject (not shown) was
obtained by weighting the PCA components by the average PCA coefficients across all breath cycles. a.u.: Arbitrary units.
doi:10.1371/journal.pone.0155084.g002
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 6/18
untrained individuals were assessed independently in order to identify the typical breathing
patterns of each participant group [36]. The input for the PCA included RC and AB volume
signals from all breath cycles of each participant, and the average PCA coefficients were multi-
plied by the Principal Components to obtain the participant’s breathing pattern. To derive the
typical breathing pattern of each group, an additional analysis was performed including RC
and AB signals from all subjects within that group. The same procedure was repeated for each
experimental task. Inter-subject variability in the PCA representations of RC and AB signals of
each group was assessed using the Variance Ratio (VR), which takes into account time and
amplitude features of the waveforms [37].
VR ¼
X
k
i¼1
X
s
j¼1
ðXij
XiÞ2=kðs1Þ
X
k
i¼1
X
s
j¼1
ðXij
XÞ2=ðks 1Þ
where kis the number of samples in the PCA representation (i.e. 1,000); sis the number of par-
ticipants in the corresponding group; X
ij
is the value at the ith sample for the jth participant;
Xi
is the average value of the ith sample over all subjects, and
Xis the average over all samples.
Statistical analysis
Repeatability of parameters in conditions with and without facemask was evaluated using
intra-class correlation coefficients (ICC). A one-way analysis of variance (ANOVA) was per-
formed to compare the anthropometric data between groups (classical, control). Paired t-tests
were used to assess the effect of facemask over repetitions of tasks 2 and 3 for each parameter.
As no significant differences were found (all: p >0.20), data from repetitions with and without
facemask were pooled before further analysis, including PCA. In order to investigate group dif-
ferences during each task, a 1-way ANOVA was applied, using group (classical, control) as
between-subject factor, to each dependent variable: respiratory frequency (Fres), time of inspi-
ration (Ti), percentage of rib cage contribution to total lung volume (%RC), phase angle and
time shift between RC and AB, correlation coefficient between RC and AB, percentage of time
and volume in paradoxical motion of RC and AB, peak and mean airflow, and total volume
excursion. An additional 2-way repeated measures ANOVA was performed on the same
dependent variables in order to assess changes between breathing and singing, with task (quiet
breathing, Waltzing Matilda, own piece) as within-subject factor and group (classical, control)
as between-subject factor. Duncan’s post-hoc test was used where appropriate with correction
for multiple comparisons. Results are reported as mean ± standard error of the mean (SEM).
Results
Acceptable repeatability was observed in all parameters assessed for tasks performed with and
without the facemask (ICC >0.75). This supports the absence of an effect of the facemask on
breathing strategy and consistency of the measures between separate trials. No differences were
found in the demographic data between groups (see Table 1, 1-way ANOVA–no effect for
group: Classical vs. Control Mean(SD); age 41.9(18.2) vs. 33.7(8.8) years, F(1,9) = 0.68,
p = 0.43; height 170.3(8.5) vs. 178.5(5.3) cm, F(1,8) = 2.87, p = 0.13; weight 70.0(12.7) vs. 70.5
(9.3) kg, F(1,8) = 0.00, p = 0.95; BMI 23.9(2.4) vs. 22.0(1.6), F(1,8) = 1.59, p = 0.24). Fig 3
shows representative examples of raw data recorded from a typical participant in each group,
together with the Konno-Mead plots, which represent the coordination between AB and RC
movements in the x- and y-axis, respectively. Although there were no significant differences
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 7/18
between groups for any parameter during quiet breathing (1-way ANOVA–no effect for group:
all F(1,9) <3.98, p >0.08), breathing patterns during singing differed in several key aspects.
During the two singing tasks, classical singers used a smaller percentage of RC contribution to
lung volume than untrained individuals (Fig 4, F(1,9) >28.87, p <0.001). Classical singers
also demonstrated greater positive phase angle and time shift between RC and AB (i.e. AB
before RC, F(1,9) >28.92, p <0.001), as well as greater percentage of time and volume of RC
in paradoxical motion (i.e. motion of RC in direction opposite to that expected for direction of
airflow, Fig 5, F(1,9) >7.6, p <0.05) and greater percentage of AB volume in paradoxical
motion (F(1,9) >10.93, p <0.01). As a consequence of these features, smaller correlation coef-
ficients were found between RC and AB signals of classical singers than controls during singing
Fig 3. Representative recordings of rib cage (RC), abdominal (AB) and total lung volumes of one classical singer and one untrained
individual performing each experimental task. Volume waveforms are shown for five consecutive breath cycles, with the corresponding
Konno-Mead plots representing the coordination between AB and RC movements (in the x- and y-axis respectively).
doi:10.1371/journal.pone.0155084.g003
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 8/18
(F(1,9) >5.7, p <0.05). During the singing of the standard piece (Waltzing Matilda), lower
mean airflow and lower volume excursion were observed in classical singers than controls (Fig
6, F(1,8) >8.9, p <0.05), but there was no effect of group for these parameters when partici-
pants sang the piece of their choice.
For both participant groups, in contrast to quiet breathing, singing tasks were associated
with shorter duration of inspiration (Fig 4, 2-way ANOVA–main effect for Task: F(2,18) =
51.22, p <0.001; post hoc: p <0.001), greater percentage of time of RC and AB paradoxical
motion (Fig 5, 2-way ANOVA–main effect for Task: F(2,18) >22.44, p <0.005; post hoc:
p<0.01), greater peak airflow, and greater volume excursion (Fig 6, 2-way ANOVA–main
effect for Task: F(2,16) >7.88, p <0.005; post hoc: p <0.05). The time shift between RC and
AB of classical singers was greater when singing their own piece than during quiet breathing
(2-way ANOVA–interaction Task × Group: F(2,18) = 4.43, p = 0.05; post hoc: p <0.05),
whereas no differences were found for untrained individuals (post hoc: p >0.35). AB volume
in paradoxical motion in classical singers was greater during both singing tasks than during
quiet breathing (2-way ANOVA–interaction Task × Group: F(2,18) = 9.18, p = 0.02; post hoc:
p<0.001), but not in untrained individuals (post hoc: p >0.13).
The patterns of RC and AB movements, estimated using principal component analysis
(PCA), are depicted in Fig 7. The waveforms obtained account for more than 98% of the vari-
ability of the original signals and therefore represent the typical patterns of each participant
Fig 4. Respiratory frequency (Fres), time of inspiration (Ti), percentage contribution of rib cage to total lung volume (%RC), phase angle, time
shift, and linear correlation coefficient between rib cage (RC) and abdomen (AB) volume waveforms of classical singers and untrained
individuals during each of the three tasks assessed. Mean + SEM are shown. *P<0.05, ** P<0.001 vs. untrained individuals. †P<0.05, ††
P<0.001 vs. quiet breathing.
doi:10.1371/journal.pone.0155084.g004
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 9/18
group, as well as the patterns of individual subjects. For both groups, more Principal Compo-
nents were required to represent RC and AB volume signals during singing than breathing
(Table 2, 2-way ANOVA–main effect for Task: F(2,18) = 17.65, p <0.001; post hoc:
p<0.001). On average, the patterns of classical singers required a larger number of Principal
Components than untrained individuals, but the group difference narrowly missed statistical
significance (Table 2, 2-way ANOVA–main effect for Group: F(1,9) = 4.74, p = 0.057). The
graphical presentation of PCA data shows high inter-subject variability of breathing patterns
between classical singers, whereas similar patterns were observed within the group of untrained
individuals. As a result, greater Variance Ratio was observed for classical singers than controls
(Table 2). Furthermore, classical singers showed strong asymmetry in the coordination
between RC and AB movements, as demonstrated by “open”loops in the Konno-Mead plots,
which were generally wider during singing tasks than quiet breathing. Untrained individuals,
on the other hand, repeated similar closed loops in the Konno-Mead plots during quiet breath-
ing and singing tasks, despite differences in the time of inspiratory and expiratory phases
between tasks.
This study performed an objective characterization of the breathing patterns of classical
singers and untrained individuals by means of Principal Component Analysis, in addition to a
number of features of respiratory kinematics. Results show no significant differences between
groups during quiet breathing, although the presence of small differences cannot be completely
excluded because of the small sample size. In particular, the data suggest a trend for greater
abdominal contribution in singers than untrained individuals during quiet breathing (1-way
Fig 5. Percentage of time and volume in paradoxical motion of rib cage (RC) and abdomen (AB) of classical
singers and untrained individuals during each of the three tasks assessed. Paradoxical motion is defined here
as outward movements of the volume compartment during the expiratory phase of each breath cycle. Mean+ SEM
are shown. *P<0.05, ** P<0.001 vs. untrained individuals. †P<0.05, †† P<0.001 vs. quiet breathing.
doi:10.1371/journal.pone.0155084.g005
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 10 / 18
ANOVA p = 0.08), illustrated in Figs 4and 7. During singing tasks, classical singers used con-
sistently greater percentage contribution of abdomen to total lung volume and moved the
abdomen inward prior to phonation, which resulted in higher asynchrony between movements
of the rib cage and the abdominal wall than untrained individuals. As a result, “open”loops
were observed in the Konno-Mead plots of the PCA representation of classical singers, i.e. dis-
tinct patterns of interaction between RC and AB during inspiration and expiration. These data
highlight strong manipulation (most likely voluntary) of the patterns of respiratory kinematics
by classical singers during singing tasks from the patterns naturally adopted during quiet
breathing. This argument is supported by the observation of greater phase shift between RC
and AB, greater contribution of AB to total lung volume, and greater inter-subject variability
among classical singers than untrained individuals. Taken together, these data suggests the
development of individual-specific respiratory techniques in classical singers, whereas
untrained individuals consistently repeated coordinated movements of RC and AB during
breathing and singing.
Breathing patterns during singing
The absence of group differences in respiratory frequency and duration of inspiration during
singing suggests that both groups adapted similarly to time constraints imposed by musical
rhythm. In addition, both groups showed predominance of RC contribution to total lung vol-
ume, which might be interpreted as greater contribution of RC muscles over AB muscles to
generate volume change. This would be consistent with observations that: (i) the RC covers a
Fig 6. Peak airflow, mean airflow, and volume excursion of classical singers and untrained
individuals during each of the three tasks assessed. Volume excursion was assessed as the difference
between the volume at initiation and termination of expiratory phase of each breath cycle. Mean + SEM are
shown. *P<0.05 vs. untrained individuals. †P<0.05 vs. quiet breathing.
doi:10.1371/journal.pone.0155084.g006
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 11 / 18
larger surface of the lungs, which enables small RC movements to produce relatively large
changes in alveolar pressure; and (ii) the small RC expiratory muscles, such as m. intercostales
interni and m. triangularis sterni, can provide fast and precise control of subglottal pressure,
particularly when lung volume is below functional residual capacity [10,14,17,19]. Despite the
predominance of RC motion, and consistent with the emphasis placed on abdominal breathing
in operatic singing training [9], classical singers used larger contributions of AB, i.e. smaller %
RC, than untrained individuals. On average, classical singers used 35% contribution of the
Fig 7. Typical breathing patterns of classical singers and untrained individuals extracted using
principal component analysis. The group’s typical patterns are represented in the large axes, whereas
patterns of individual participants are represented in small axes. Volume waveforms are shown with the
corresponding Konno-Mead plots of RC and AB movements. The arrowheads in the Konno-Mead plots
illustrate the time course, i.e. ascending and descending arrows correspond to inspiratory and expiratory
phases, respectively. The start of expiration phase is marked in green both in the time plots and Konno-Mead
plots. Note: The raw data shown in Fig 3 were recorded from classical singer #1 and untrained individual #4.
doi:10.1371/journal.pone.0155084.g007
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 12 / 18
abdomen during singing tasks, approximately 2.5 times the average contribution used by
untrained individuals (14%). This corroborates previous reports based on subjective interpreta-
tion of raw data, which suggested greater deformations of the abdominal wall of classical sing-
ers than untrained individuals during singing [2,33].
Despite the short time of inspiration (mean 0.7 s), classical singers used inhalation manoeu-
vres that involved complex movements of respiratory compartments: In most singers, the AB
wall began to expand prior to RC (i.e. positive phase angle), and AB peak volume occurred ear-
lier than RC peak volume at the transition from inhalation to phonation (i.e. positive time
shift). As a result, inward movement of AB started before maximum lung volume was reached,
as depicted by the raw data in Fig 3 and the PCA representations in Fig 7. Such volume shift
from AB to RC has been previously observed in classical singers in the transition from inspira-
tion to phonation phase [2]. One interpretation of this early movement of the abdominal wall
is that it can aid inspiration by stabilisation of the central tendon (control of the descent of the
diaphragm) to enable the diaphragm to generate greater effect on the rib cage, i.e. rib elevation
and lateral expansion [38]. This would be particularly important in standing position, where
the gravitational effect on the abdominal viscera tends to lower the abdominal contents and
thus the diaphragm position, shortening its muscle fibres. Moreover, the inward displacement
of AB moves the diaphragm towards the thorax, which improves its position in the length-ten-
sion curve for the production of rapid changes in airflow, as a lengthened diaphragm yields
more effective translation of muscle tension into transdiaphragmatic pressure [2,39–41]. Fur-
thermore, as a result of the expansion of RC, pre-phonatory transfer of lung volume from AB
to RC generates greater respiratory recoil forces and increases contractile force of expiratory
rib cage muscles [4,42]. During phonation, contraction of abdominal muscles would elevate
intra-abdominal pressure [43,44] and thus allow more efficient control of subglottal pressure
required for sound production. Supporting this argument, greater activation of the obliquus
internus and externus abdominis, and rectus abdominis muscles has been observed in profes-
sional operatic singers than students during singing tasks [24]. This has been related to changes
in peaks of the sound power spectrum (known as formant frequencies) that are considered
reflective of greater classical voice quality [6,28,45].
In the current study, strong agreement was observed in respiratory kinematics between
singing tasks performed with and without a facemask. This demonstrates reliability of the
experimental set up and repeatability of the breathing strategies used by both groups
[30,31,46]. It should be noted that intra-subject repeatability of breathing patterns was not lim-
ited to rhythm-related constraints to the duration of inspiration and phonation phases that has
been previously reported [23,46], but was also observed for the dynamics of respiratory kine-
matics (e.g. phase angle between RC and AB). This repeatability most likely reflects consistency
of personal singing skills and respiratory strategies.
Table 2. Number of Principal Components (PC, mean ±SD) and Variance Ratio (VR) of PCA representations of RC and AB volume signals for clas-
sical singers and untrained (control) individuals.
Parameter Quiet Breathing Waltzing Matilda Own Piece
Classical Control Classical Control Classical Control
Number of PCs 2.86 ±1.07 2.25 ±0.5 5.43 ±1.62 3.75 ±0.5 5.86 ±1.57 4.75 ±0.5
VR RC 0.444 0.056 0.231 0.049 0.303 0.131
VR AB 0.420 0.299 0.324 0.218 0.362 0.440
Note: PCA: Principal Component Analysis. RC: Rib cage. AB: Abdomen.
doi:10.1371/journal.pone.0155084.t002
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 13 / 18
On the other hand, high inter-subject variability of respiratory kinematics has been com-
monly reported among classical singers [24,29]. During performances of the vocal exercise
known as messa di voce, in which the loudness of a note is gradually increased and then
decreased without changing other voice features such as pitch or timbre, singers with long per-
forming experience demonstrated individual-specific patterns of respiratory kinematics, as
opposed to the more stereotypic behaviour of less trained singers [47]. The breathing patterns
shown in Fig 7 demonstrate similar observations during quiet breathing and the performance
of full songs (i.e. Waltzing Matilda and the participant’s own piece of choice). Although the
breathing patterns were similar among all untrained individuals, professional classical singers
showed high degree of heterogeneity. This resulted in greater Variance Ratio and individual-
specific breathing dynamics, as clearly shown by the Kono-Mead plots (Fig 7). As an example,
singer #5 was the only one to demonstrate inward movements of RC at the start of inspiration,
despite previous suggestion that this is a common behaviour among classical singers [4]. More-
over, singer #4 displayed a pattern similar to that of untrained individuals, despite having more
than 21 years of performing experience. Taken together, these data highlight that although it is
presumed that breath management techniques may provide physiological and mechanical ben-
efits that optimise classical voice quality (through active modification of respiratory kinematics
from the patterns spontaneously adopted by untrained individuals), these are not uniformly
used by professional singers. This may imply that voice quality can be optimised by a range of
mechanisms in addition to these standard techniques, e.g. dynamic changes in laryngeal and
glottal configuration. This would partially explain the limited correlation between acoustic
parameters and respiratory movements reported in previous studies [4].
Breathing and singing
In addition to time constraints related to musical rhythm, singing tasks require more rapid
inspiration and longer expiration for sustained utterances than quiet breathing, and this often
results in end-expiratory volumes below functional residual capacity [48]. Accordingly, the
current results indicate that classically trained and untrained singers adjusted the breathing
patterns to singing task demands by decreased duration of inspiration, greater peak airflow,
and greater volume excursion than during quiet breathing. However, changes in the time shift
between RC and AB were observed only in classical singers. This suggests untrained individuals
used similar strategies of respiratory movements during quiet breathing and singing tasks.
Assessment of PCA representations demonstrates that, despite substantial differences between
the time profiles of respiratory kinematics between tasks, the coordination between RC and AB
of untrained individuals remained virtually unchanged. This observation agrees with and
extends the findings of (i) significant correlation between the slopes of the Konno-Mead plots
of RC and AB movements of untrained individuals during quiet breathing and reading tasks
[49]; and (ii) similar Konno-Mead plots (based on visual inspection of raw data) when
untrained individuals performed speaking, reading and singing tasks [33].
In contrast to untrained individuals, classical singers demonstrated greater time shift
between RC and AB during singing than quiet breathing, and this was associated with greater
AB volume in paradoxical motion. These findings suggest independent coordination of RC
and AB muscles in classical singers, particularly in the transition from inspiration to phona-
tion. Early inward movements of AB increase intra-abdominal pressure and diaphragm eleva-
tion prior to phonation [2]. This enables quick airway modulation during utterances and
increases glottal efficiency, i.e. greater ratio between acoustic and aerodynamic power [6,50].
Moreover, classical singers often use most of their inspiratory vital capacity when singing [2],
generating stronger recoil forces than untrained individuals, who are usually limited to
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 14 / 18
volumes around the mid-range of vital capacity [33]. This enhanced efficiency could explain
the current observation of lower mean airflow used by classical singers than untrained individ-
uals during the performance of a similar singing task (i.e., Waltzing Matilda), as well as previ-
ous reports of lower subglottal pressure in classical singers than both country and musical
theatre singers during speaking and singing tasks [51,52]. In line with this argument, classical
singers can increase sound pressure level without changes in respiratory effort when singing
with supported compared with unsupported voice [6]. In that study, the increase was attributed
to changes in laryngeal and glottal configuration, such as lowering the larynx and tight closing
the glottis, which was also associated with clearer voice quality. Despite this difference during
the standard song, when required to perform at high vocal intensity, classical singers can
develop greater airflow than non-singers. With a more efficient use of the vocal tract, this
results in greater sound pressure level for the same lung pressures [53,54]. Although the current
results do not imply the existence of an “optimal”method of training the singing voice, it
underpins the importance of breath kinematics for classical singers, particularly the indepen-
dent control of RC and AB movements.
One issue to consider when assessing breathing patterns in different individuals is that body
type affects breathing and speech [55], and previous studies have reported greater mean and
peak airflow in male than female singers, particularly at high pitches [6]. Hence, group differ-
ences in mean airflow in the current study might be explained, at least in part, by the predomi-
nance of females in the present group of classical singers. Although the current sample size
does not allow sub-grouping based on gender, assessment of individual averages revealed that
the male singers produced the highest mean airflow within the classical group (52 ± 25 mL/s).
Two female singers demonstrated intermediate values (43 ± 22 mL/s) and the remaining two
females demonstrated lower values (15 ± 11 mL/s). As the group average of the untrained indi-
viduals was substantially greater than all classical singers (114 ± 42 mL/s), gender effects cannot
fully account for the group differences. Moreover, no significant differences were found in age,
height, weight, or BMI between groups. Considering that two classical singers were more than
60 years old, it is important to consider that physiological age-related changes such as smaller
vital capacities, reduced recoil of lung tissue, and reduced muscle strength may limit the range
of vocal intensities in the elderly, potentially affecting vocal pitch, loudness, and quality [56].
The effects of these changes on the singing voice are highly variable, and depend on the level of
vocal training. In non-singers, the fundamental frequency of voice is substantially lower in
elderly compared to young adults, but not in elder professional singers [57], who are able to
generate oral pressures that are similar to those of younger adults [58].
It is important to note the potential limitations of inductance plethysmography for record-
ing respiratory kinematics. This device can only detect changes in the cross-sectional area of
the cavities at the level of the bands and have limited capacity to detect distortion of rib-cage
shape [59] or regional abdominal behaviour [60]. Despite this limitation, several methodologi-
cal studies have demonstrated high accuracy of inductance plethysmography for the analysis of
respiratory waveforms during quiet breathing and exercise [61,62].
Conclusion
No significant differences were observed between the patterns of respiratory kinematics of
untrained individuals and classical singers during quiet breathing, although there was a trend
for greater abdominal contribution in singers than untrained individuals. In contrast, each
group demonstrated distinct adaptations during singing tasks. Untrained individuals displayed
minimal differences in the coordination between rib cage and abdominal movements with
singing, which suggests similar respiratory patterns during both breathing and singing.
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 15 / 18
Although there was some variation between participants, most classical singers demonstrated
greater contribution of the abdomen to total lung volume than untrained individuals during
singing tasks, and this was associated with pre-phonatory inward movements of the abdominal
wall and a greater degree of independence in the movements of the rib cage and abdomen. This
would increase the length and the pressure-generating capacity of rib cage expiratory muscles
and elevate intra-abdominal pressure to improve the control of subglottal pressure during long
utterances. These adaptations have been associated with changes in sound power spectrum and
may have implications for voice quality, as commonly advocated by classical singing teachers
and professionals.
Supporting Information
S1 Dataset. All parameters used in the data analysis, calculated for each individual during
each task.
(XLSX)
Acknowledgments
The authors thank Brenton Keates, Leanne Hall and Andrew Claus for assistance with data col-
lection and Kylie Tucker for fine-wire insertion in some participants.
Author Contributions
Conceived and designed the experiments: PH. Performed the experiments: PH WH. Analyzed
the data: SS WH. Wrote the paper: SS WH PH.
References
1. Prisk GK, Hammer J, Newth CJL. Techniques for measurement of thoracoabdominal asynchrony.
Pediatr Pulmonol. 2002 Nov 6; 34(6):462–72. PMID: 12422344
2. Watson PJ, Hixon TJ. Respiratory kinematics in classical (opera) singers. J Speech Hear Res. 1985
Mar; 28(1):104–22. PMID: 3157022
3. Thomasson M, Sundberg J. Lung volume levels in professional classical singing. LogopedPhoniatr
Vocol. Informa UK Ltd UK; 1997; 22(2):61–70.
4. Thorpe CW, Cala SJ, Chapman J, Davis PJ. Patterns of breath support in projection of the singing
voice. J Voice. Elsevier; 2001; 15(1):86–104. PMID: 12269638
5. Tang Y, Turner MJ, Yem JS, Baker AB. Calibration of pneumotachographs using a calibrated syringe. J
Appl Physiol. 2003 Aug; 95(2):571–6. PMID: 12704091
6. Griffin B, Woo P, Colton R, Casper J, Brewer D. Physiological characteristics of the supported singing
voice. A preliminary study. J Voice. 1995 Mar; 9(1):45–56. PMID: 7757150
7. Sand S, Sundberg J. Reliability of the term “support”in singing. Logoped Phoniatr Vocol. 2005 Jan; 30
(2):51–4. PMID: 16147223
8. Ivanenko YP. Coordination of Locomotion with Voluntary Movements in Humans. J Neurosci. 2005
Aug 3; 25(31):7238–53. PMID: 16079406
9. Spillane KW. Breath support directives used by singing teachers: a Delphi study. The NATS Journal.
Columbia University; 1989; 45:9.
10. De Troyer A, Kirkwood PA, Wilson TA. Respiratory Action of the Intercostal Muscles. Physiol Rev.
2005 Apr; 85(2):717–56. PMID: 15788709
11. Tresch MC, Saltiel P, Bizzi E. The construction of movement by the spinal cord. Nat Neurosci. 1999
Feb; 2(2):162–7. PMID: 10195201
12. Watson PJ, Hixon TJ, Stathopoulos ET, Sullivan DR. Respiratory kinematics in female classical sing-
ers. J Voice. 1990 Mar 22; 4:120–8.
13. Winter DA, Yack HJ. EMG profiles during normal human walking: stride-to-stride and inter-subject vari-
ability. Electroencephalogr Clin Neurophysiol. 1987 Nov; 67(5):402–11. PMID: 2444408
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 16 / 18
14. De Troyer A, Legrand A, Gevenois P- A, Wilson TA. Mechanical advantage of the human parasternal
intercostal and triangularis sterni muscles. J Physiol. Physiological Soc; 1998; 513(3):915–25.
15. Bouhuys A, Proctor DF, Mead J. Kinetic aspects of singing. J Appl Physiol. 1966 Mar; 21(2):483–96.
PMID: 5934452
16. Watson PJ, Hoit JD, Lansing RW, Hixon TJ. Abdominal muscle activity during classical singing. J
Voice. Elsevier; 1989; 3(1):24–31.
17. Estenne M, Zocchi L, Ward M, Macklem PT. Chest wall motion and expiratory muscle use during pho-
nation in normal humans. J Appl Physiol. Am Physiological Soc; 1990; 68(5):2075–82. PMID: 2361909
18. Pettersen V, Westgaard RH. The Activity Patterns of Neck Muscles in Professional Classical Singing. J
Voice. 2005 Jun; 19(2):238–51. PMID: 15907438
19. Han JN, Gayan-Ramirez G, Dekhuijzen R, Decramer M. Respiratory function of the rib cage muscles.
Eur Respir J. 1993 May; 6(5):722–8. PMID: 8519384
20. Macdonald I, Rubin JS, Blake E, Hirani S, Epstein R. An investigation of abdominal muscle recruitment
for sustained phonation in 25 healthy singers. J Voice. 2012 Nov; 26(6):815.e9–16.
21. Baken RJ, Cavallo SA, Weissman KL. Chest wall movements prior to phonation. J Speech Hear Res.
1979 Dec; 22(4):862–71. PMID: 513693
22. Hixon TJ, Watson PJ, Harris FP, Pearl NB. Relative volume changes of the rib cage and abdomen dur-
ing prephonatory chest wall posturing. J Voice. Elsevier; 1988; 2(1):13–9.
23. McFarland DH, Smith A. Effects of vocal task and respiratory phase on prephonatory chest wall move-
ments. J Speech Hear Res. 1992 Oct; 35(5):971–82. PMID: 1447931
24. Pettersen V, Westgaard RH. Muscle activity in professional classical singing: a study on muscles in the
shoulder, neck and trunk. Logoped Phoniatr Vocol. 2004 Jan; 29(2):56–65. PMID: 15260181
25. Iwarsson J. Effects of inhalatory abdominal wall movement on vertical laryngeal position during phona-
tion. J Voice. Elsevier; 2001; 15(3):384–94. PMID: 11575635
26. Pettersen V, Westgaard RH. The association between upper trapezius activity and thorax movement in
classical singing. J Voice. 2004 Dec; 18(4):500–12. PMID: 15567051
27. Foulds-Elliott SD, Thorpe CW, Cala SJ, Davis PJ. Respiratory function in operatic singing: effects of
emotional connection. Logoped Phoniatr Vocol. 2000; 25(4):151–68. PMID: 11286437
28. Sundberg J. Articulatory interpretation of the "singing formant". J Acoust Soc Am. 1974 Apr; 55(4):838–
44. PMID: 4833080
29. Collyer S, William TC, Callaghan J, Davis PJ. The influence of fundamental frequency and sound pres-
sure level range on breathing patterns in female classical singing. J Speech Lang HearRes. ASHA;
2008; 51(3):612. doi: 10.1044/1092-4388(2008/044) PMID: 18506039
30. Thomasson M, Sundberg J. Consistency of phonatory breathing patterns in professional operatic sing-
ers. J Voice. 1999 Dec; 13(4):529–41. PMID: 10622519
31. Thomasson M, Sundberg J. Consistency of inhalatory breathing patterns in professional operaticsing-
ers. J Voice. 2001 Sep; 15(3):373–83. PMID: 11575634
32. Collyer S, Kenny DT, Archer M. The effect of abdominal kinematic directives on respiratory behaviour
in female classical singing. Logoped Phoniatr Vocol. 2009 Jan; 34(3):100–10. doi: 10.1080/
14015430903008780 PMID: 19479619
33. Hixon TJ. Kinematics of the chest wall during speech production: volume displacements of the rib cage,
abdomen, and lung. J Speech Hear Res. 1973 Mar; 16(1):78–115. PMID: 4267384
34. Hoit JD, Jenks CL, Watson PJ, Cleveland TF. Respiratory function during speaking and singing in pro-
fessional country singers. J Voice. Elsevier; 1996; 10(1):39–49. PMID: 8653177
35. Konno K, Mead J. Measurement of the separate volume changes of rib cage and abdomen during
breathing. J Appl Physiol. 1967 Mar; 22(3):407–22. PMID: 4225383
36. Reilly KJ, Moore CA. Respiratory movement patterns during vocalizations at 7 and 11 months of age. J
Speech Lang Hear Res. 2009 Feb; 52(1):223–39. doi: 10.1044/1092-4388(2008/06-0215) PMID:
18695025
37. hug F, Turpin NA, Guével A, Dorel S. Is interindividual variability of EMG patterns in trained cyclists
related to different muscle synergies? J Appl Physiol. 2010 Jun 2; 108(6):1727–36. doi: 10.1152/
japplphysiol.01305.2009 PMID: 20299611
38. De Troyer A. Respiratory effect of the lower rib displacement produced by the diaphragm. J Appl Phy-
siol. 2012 Feb; 112(4):529–34. doi: 10.1152/japplphysiol.01067.2011 PMID: 22134697
39. Cavallo SA, Baken RJ. Prephonatory laryngeal and chest wall dynamics. J Speech Hear Res. 1985
Mar; 28(1):79–87. PMID: 3982000
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 17 / 18
40. Winslow C, Rozovsky J. Effect of spinal cord injury on the respiratory system. Am J Phys Med Rehabil.
2003 Oct; 82(10):803–14. PMID: 14508412
41. Smith J, Bellemare F. Effect of lung volume on in vivo contraction characteristics of human diaphragm.
J Appl Physiol. 1987 May; 62(5):1893–900. PMID: 3597263
42. Abe T, Kusuhara N, Yoshimura N, Tomita T, Easton PA. Differential respiratory activity of four abdomi-
nal muscles in humans. J Appl Physiol. Am Physiological Soc; 1996; 80(4):1379–89. PMID: 8926270
43. Hodges PW, Gandevia SC. Activation of the human diaphragm during a repetitive postural task. J Phy-
siol. 2000 Jan 1; 522 Pt 1:165–75. PMID: 10618161
44. Hodges PW, Gandevia SC. Changes in intra-abdominal pressure during postural and respiratory acti-
vation of the human diaphragm. J Appl Physiol. 2000 Sep; 89(3):967–76. PMID: 10956340
45. Leanderson R, Sundberg J. Breathing for singing. J Voice. Elsevier; 1988; 2(1):2–12.
46. Collyer S, Davis PJ. Effect of facemask use on respiratory patterns of women in speech and singing. J
Speech Lang Hear Res. 2006 Apr; 49(2):412–23. PMID: 16671853
47. Titze IR, Long R, Shirley GI, Stathopoulos ET, Ramig LO, Carroll LM, et al. Messa di voce: an investiga-
tion of the symmetry of crescendo and decrescendo in a singing exercise. J Acoust Soc Am. 1999 May;
105(5):2933–40. PMID: 10335642
48. Binazzi B, Lanini B, Bianchi R, Romagnoli I, Nerini M, Gigliotti F, et al. Breathing pattern and kinematics
in normal subjects during speech, singing and loud whispering. Acta Physiol. 2006 Mar; 186(3):233–
46.
49. Mandros C, Kampolis C, Kalliakosta G, Tzelepis GE. Relative contributions of the ribcage and abdo-
men to lung volume displacement during speech production. Eur J Appl Physiol. 2008 Mar; 102
(4):425–30. PMID: 17985153
50. Carroll LM, Sataloff RT, Heuer RJ, Spiegel JR, Radionoff SL, Cohn JR. Respiratory and glottal effi-
ciency measures in normal classically trained singers. J Voice. Elsevier; 1996; 10(2):139–45. PMID:
8734388
51. Cleveland TF, Stone RE Jr, Sundberg J, Iwarsson J. Estimated subglottal pressurein six professional-
country singers. J Voice. 1997 Dec; 11(4):403–9. PMID: 9422273
52. Björkner E. Musical Theater and Opera Singing—Why So Different? A Study of Subglottal Pressure,
Voice Source, and Formant Frequency Characteristics. J Voice. 2008 Sep; 22(5):533–40. PMID:
17485197
53. Titze I, Sundberg J. Vocal intensity in speakers and singers. J Acoust Soc Am. 1992 Jan 1;:1–11.
54. Akerlund L, Gramming P. Average loudness level, mean fundamental frequency, and subglottal pres-
sure: comparison between female singers and nonsingers. J Voice. 1994 Sep; 8(3):263–70. PMID:
7987429
55. Hoit JD, Hixon TJ. Body type and speech breathing. J Speech Hear Res. 1986 Sep; 29(3):313–24.
PMID: 3762095
56. Hodge FS, Colton RH, Kelley RT. Vocal intensity characteristics in normal and elderly speakers. J
Voice. 2001 Dec; 15(4):503–11. PMID: 11792026
57. Brown WS Jr., Morris RJ, Hollien H, Howell E. Speaking fundamental frequency characteristics as a
function of age and professional singing. J Voice. 1991.
58. Morris RJ, Brown WS Jr. Age-related voice measures among adult women. J Voice. 1987.
59. Chihara K, Kenyon CM, Macklem PT. Human rib cage distortability. J Appl Physiol. 1996 Jul; 81
(1):437–47. PMID: 8828696
60. Boynton BR, Barnas GM, Dadmun JT, Fredberg JJ. Mechanical coupling of the rib cage, abdomen,
and diaphragm through their area of apposition. J Appl Physiol. 1991 Mar; 70(3):1235–44. PMID:
2032989
61. Carry P-Y, Baconnier P, Eberhard A, Cotte P, Benchetrit G. Evaluation of Respiratory Inductive
Plethysmography Accuracy for Analysis of Respiratory Waveforms. CHEST. American College of
Chest Physicians; 1997; 111(4):910–5. PMID: 9106568
62. Aliverti A, Ghidoli G, DellacàRL, Pedotti A, Macklem PT. Chest wall kinematic determinants of dia-
phragm length by optoelectronic plethysmography and ultrasonography. J Appl Physiol. 2003 Feb; 94
(2):621–30. PMID: 12391129
Breathing and Singing
PLOS ONE | DOI:10.1371/journal.pone.0155084 May 9, 2016 18 / 18
