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Bilateral Song Production in Domestic Canaries
Roderick A. Suthers,1 Eric Vallet,2 Aure´ lie Tanvez,2 Michel Kreutzer2
1 Medical Science and Department of Biology, Indiana University, Bloomington, Indiana 47405
2 Laboratoire d’Ethologie et Cognition Compare´ es, Universite´ Paris 10-Nanterre, Baˆ timent H, 200,
avenue de la re´ publique, 92001 Nanterre cedex
Received 8 July 2003; accepted 15 January 2004
ABSTRACT: We studied the mechanism of song
production in the outbred common or domestic canary
(Serinus canaria). The contribution that each side of the
syrinx makes to song was investigated by observing the
effect of unilaterally occluding the left or right primary
bronchus, followed by section of the ipsilateral branch of
the tracheosyringeal nerve. In other birds with a bilaterally
intact vocal system we monitored airflow through
each side of the syrinx, together with subsyringeal pressure,
during spontaneous song. Song production by domestic
canaries is not strongly lateralized as it is in the
conspecific song-bred waterslager strain. Some syllables
are produced entirely on the left or right side of the
syrinx, whereas others contain sequential contributions
from each side. Low fundamental frequencies are produced
with the left syrinx and high frequencies by the
right syrinx, increasing the frequency range of domestic
canary song compared to that of the waterslager strain.
Midrange frequencies can be generated by either side.
Syllables at repetition rates below about 25 s
1 were
accompanied by minibreaths, which were usually bilateral.
Unilateral minibreaths were typically on the left
side. At higher syllable repetition rates, minibreaths
were replaced by a respiratory pattern of pulsatile expiration.
Our data show that strong unilateral dominance
in song production, present in the waterslager
strain, is not a trait of the species as a whole and that the
pattern of song lateralization can be altered by selective
breeding for particular song characteristics. © 2004
Wiley Periodicals, Inc. J Neurobiol 60: 381–393, 2004
Keywords: birdsong; neural lateralization; syrinx; vocalization
INTRODUCTION
The canary (Serinus canaria) has had an influential
role in the neurobiology of birdsong, but information
on this species has come largely from a single genetic
strain—the waterslager canary—that was bred by aviculturists
for the low pitched, liquid quality of its
song. Using this strain, Nottebohm and Nottebohm
(1976) demonstrated that about 85% or more of its
song is sung on the left side of its bipartite syrinx,
making it one of the first and most robust nonhuman
examples of a lateralized neural control of behavior.
A similar degree of song lateralization has not
been found in the other species of songbirds that
have subsequently been studied (Williams et al.,
1992; Suthers, 1997, 1999; Suthers et al., 1999).
The presence of genetically distinct canary strains
with distinctive songs provides an opportunity to
investigate the extent to which the motor mechanisms
for singing differ between strains of a single
species, and the relationship of this motor variation
to the acoustic properties of strain-specific songs. Is
unilateral dominance in song production a characteristic
of the species as a whole or does it vary
among different strains? Can differences in vocal
mechanisms help in understanding interstrain differences
in song learning (Mundinger, 1995), or
Correspondence to: R. Suthers (suthers@indiana.edu).
Contract grant sponsor: NIH-NINDS; contract grant number:
R01 NS29467 (R.S.).
© 2004 Wiley Periodicals, Inc.
DOI 10.1002/neu.20040
Published online 15 June 2004 in Wiley InterScience (www.
interscience.wiley.com).
381
why adult males commonly produce own-strain
song features and rarely others?
Although the genetic diversity of domestic canaries
limits the ability to draw conclusions about the
genetic basis of their behavioral traits, their song is
more similar to that of its wild island canary ancestors
than to that of the waterslager or other song-bred
strains. Unlike waterslager canaries, the common domestic
canary is an outbred strain that has not been
subjected to as much artificial selection for either a
particular song or appearance. The experiments reported
here are a first step in comparing song motor
mechanisms of the outbred domestic and song-bred
canary strains. The motor correlates of a special class
of high repetition rate, broad band canary syllables
(called sexy syllables or A-syllables) that are particularly
effective in eliciting copulation solicitation displays
from females (Vallet and Kreutzer, 1995), are
described elsewhere (Suthers et al., 2004).
METHODS
The male domestic canaries used in these experiments were
reared in aviaries with other conspecifics at the University
of Paris X, Nanterre, France. Prior to an experiment, birds
were brought into breeding condition by moving them from
short to long day (16:8 L/D) photoperiods.
Disabling One Side of the Syrinx
The effect on song of disabling one side of the syrinx was
studied in eight 2-year-old males. Either the left or right side
of the syrinx was silenced by blocking airflow through the
corresponding primary bronchus and denervating the syringeal
muscles on the same side of the syrinx.
Unilateral Bronchial Plugs and Neurotomy. After recording
their song repertoire, each bird was anesthetized with
chloropent (3.8 to 4.0
L g
1, i.m.; Fort Dodge Laboratories).
The syrinx and bronchi were exposed by a ventral
midline incision in the membrane of the interclavicular air
sac, which contains these structures. Dental impression medium
(Super-Dent Impra-mix light; Rugby Labs, Inc.) was
injected into one primary bronchus (four birds on each side)
through a 26 ga hypodermic needle inserted between two
bronchial rings. To reduce the possibility of the plug becoming
displaced, a small amount of tissue adhesive (Vetbond;
3M Animal Care Products, St. Paul, MN) was applied
to one end of it in some birds or a tab of impression medium
was allowed to extend out of the bronchus through the hole
made by the injection needle. The incision in the interclavicular
membrane was then closed and made airtight with
sutures and a small amount of tissue adhesive. The bird was
then allowed to recover from the anesthesia and returned to
its cage. Canaries resumed singing within about 2 or 3 days
after surgery.
Eight to 16 days after a bronchus was plugged, the same
birds were anesthetized again with chloropent, as described
above. An incision was made in the skin along the ventrolateral
surface of the neck and the trachea was exposed
about midway along its length. Each side of the syrinx is
separately innervated by an ipsilateral tracheosyringeal
branch of the hypoglossal nerve, which travels along each
side of the trachea. A 4 mm long segment of this nerve,
together with its neural sheath, was removed on the side
innervating the syringeal muscles ipsilateral to the bronchial
plug, which was not disturbed. Birds typically resumed
singing within a day after this minor surgery.
Song Recording and Analysis. Pre- and postoperative
songs were recorded on a cassette recorder (model PMD 20;
Marantz) using a condenser microphone (model EMU 4535;
LEM Industries). Each individual was housed singly in a
cage during each recording session but had visual and
acoustic interactions with other adults in the same room. We
selected this recording design because it has been shown
that spontaneous song by isolated domestic canaries (e.g., in
sound attenuation chambers) is not a reliable index of their
song repertoire during social interactions (Kreutzer et al.,
1999). Thus each individual was recorded in the presence of
other birds at least two times per day during about 1 week.
Each recording session lasted about 15 min. More than 80
songs were recorded from each individual.
Phrases of each syllable type were digitized (sample rate
22 kHz, 16 bits) from the original recording using Sound
Edit 16 v 2 (Macromedia) software, and the maximum and
minimum frequency, duration, and repetition rate were measured
with cursors from the sonograms of each syllable
type. A song was defined as a bout of vocalization lasting at
least 0.7 s (Gu¨ttinger et al., 1978). About 80 preoperative
and 80 postoperative songs were analyzed for each male.
Previous studies on more than 30 adult male domestic
canaries, recorded in similar conditions, demonstrated that
this sample size is sufficient to obtain a bird’s full repertoire
(E. Vallet et al., unpublished data).
Physiological Correlates of Sound
Production in the Intact Syrinx
The mechanism of song production in the bilaterally intact
syrinx was studied in three additional males by monitoring
the airflow through each side of the syrinx and respiratory
pressure during spontaneous song. The methods for this
experiment are described elsewhere (Suthers, 1990; Suthers
et al., 1994) and will only be summarized here.
Bronchial Airflow. Access to the bronchi was obtained via
a midline ventral incision in the interclavicular air sac as
described above in the section Unilateral Bronchial Plugs
and Neurotomy. The rate of airflow through each side of the
syrinx was measured by implanting a microbead thermistor
(BB07PA302N; Thermometrics) in each primary bronchus.
382 Suthers et al.
A thermistor bead was inserted through a small hole in the
membrane between bronchial cartilages several rings below
the syrinx and positioned near the middle of the bronchial
lumen. The thermistor was held in place with a drop of
tissue adhesive on the outside of the bronchus. A pair of fine
wires from each thermistor exited the interclavicular air sac
through the incision, which was then carefully sealed, and
routed subcutaneously to microconnectors on a backpack.
Flexible wires from the backpack exited through the top of
the cage to signal conditioning and recording instruments. A
feedback circuit maintained the thermistors at a constant
temperature and the current required to do this provided a
nonlinear measure of the rate of airflow.
Respiratory Pressure. The direction of airflow was determined
from the respiratory pressure, which was measured
simultaneously via a silastic cannula (ID 1.02 mm, OD 2.16
mm, length 55 mm) inserted into a cranial thoracic air sac
and connected to a miniature piezoresistive pressure transducer
(Fujikura model FPM-02PG) mounted on the backpack.
After recovering from surgery the bird was able to
move about freely in its home cage on a wire tether attached
to its backpack.
Data Recording. Preoperative song was recorded as described
above. Song after surgery was recorded by a condenser
microphone (model AT835b; Audio Technica) positioned
about 0.5 m in front of the bird. Song, airflow
through the left and right primary bronchi, and cranial
thoracic air sac pressure were recorded concurrently on
separate channels of DAT tape using a data recorder (TEAC
model RD135T; bandwidth DC–10 kHz/channel).
Data Analysis. For analysis, the taped data were reproduced
at half speed and converted into “Signal” (Engineering
Design) files with a real-time digitization rate of 40 kHz
(Data Translation, 2821-G) per channel. Sound spectrograms
were computed using an FFT length of 512 points
with a Hanning window, giving a frequency resolution of 86
Hz and temporal resolution of 11.6 ms, unless otherwise
indicated. Syllable fundamental bandwidth and frequency
range were determined at 30 dB below the peak amplitude
of power spectra.
RESULTS
Effect on Song of Silencing One Side of
Syrinx
In order to assess the relative contribution each side of
the syrinx makes to song, we compared the song
repertoires of two groups of four birds before and
after silencing one side of the syrinx by filling the
bronchus with dental impression medium and denervating
the ipsilateral syringeal muscles.
Repertoire Size. Preoperative repertoires ranged
from 22 to 42 syllable types. After a unilateral bronchus
plug and nerve section, the majority of syllables
in the preoperative repertoire were lost but many new
syllables appeared (Table 1). The size of the postoperative
repertoire increased in half of both the leftand
right-side operated birds, but decreased in the
other half of each of these groups. The repertoire size
changed by only one or two syllables for half the birds
in each of these experimental groups. Of the two
remaining right-side operated birds, one repertoire
increased by eight syllables (26%) and the other
decreased by 20 syllables (
51%). Repertoire size
decreased in both of the remaining left-side operated
birds by six (
27%) and eight (
25%) syllables,
respectively. The mean repertoire size of each group
changed little, regardless of which side of the syrinx
remained intact (Table 1).
Subrepertoire of Multinote Syllables. The total number
of syllables composed of two or more notes in the
song repertoires decreased markedly after surgery in
seven out of eight birds. The subrepertoire of these
syllables decreased more than 50% from its preoperative
size in two right-side operated (79 and 97%
decrease) and three left-side operated (55 to 87%
decrease) birds. In a third right-side operated bird this
syllable type decreased 22%, but increased 6% in the
fourth bird. The fourth bird operated on the left side
had a 29% decrease in the number of complex syllables
(Table 2).
Three of four birds singing with their left syrinx
(right side plugged and denervated) continued to produce
some multinote syllables at repetition rates
greater than 15 s
1 (Table 2). None of these postoperative,
high repetition rate, unilateral syllables
Table 1 Effect on Repertoire Size of Silencing One
Side of Syrinx with Bronchus Plug and Ipsilateral
Nerve Section
Bird
Side
Operated
Preoperative
Repertoire
Postoperative
Repertoire*
1 Right 26 28 (4)
2 Right 31 39 (2)
3 Right 42 41 (4)
14 Right 39 19 (5)
Mean  SD: 34.5  7.3 31.8  10.2
4 Left 29 31 (1)
6 Left 32 24 (0)
9 Left 38 39 (3)
10 Left 22 16 (1)
Mean  SD: 30.3  6.6 27.5  9.8
*Preoperative syllables in parentheses.
Song Production in Domestic Canaries 383
matched syllables present in the preoperative repertoire.
None of the birds singing with their right syrinx
(left side plugged and denervated) produced a syllable
that clearly contained more than one note (Table 2).
Conserved Syllables. In all birds, the majority of
postoperative syllables were different than those in
the preoperative repertoire, regardless of which side
of the syrinx was disabled. Some syllables from the
preoperative repertoire were retained, however, after
the unilateral bronchial plug and nerve section (Table
1). The number of syllables retained was larger in
birds with a functional left syrinx than in those with a
functional right syrinx (except bird 9) (Table 1).
Those syllables that were not affected by plugging
and denervating one side of the syrinx were presumably
sung entirely on the intact side before, as well as
after, surgery. Some of these conserved syllables were
simple, single note frequency sweeps [e.g., Fig. 1
syllables (c,e,h)], but a few were low repetition rate,
multinote syllables [e.g., Fig. 1 syllables (a,d,f,g)].
The highest repetition rate of conserved unilateral
multinote syllables was about 13 s
1 [Fig. 1, syllable
(g)]. Syllables having the most complex frequency
modulations [e.g., Fig. 1, syllables (a,d)] originated in
the right syrinx, but our sample is too small to determine
if this is a functional specialization of the right
side.
Partially Conserved Syllables. Some multinote syllables
in the preoperative repertoires were partially
conserved after bronchus plugging or plugging and
neurotomy (Figs. 2 and 3). These syllables presumably
contained notes arising on different sides of the
intact syrinx, so that after one side was disabled only
notes on the intact side remained. It is noteworthy that
the tempo of the original phrase was retained so that
the missing notes were replaced by silent periods and
the conserved notes were sung at the same repetition
rate as before surgery (Figs. 2 and 3). The three note
syllable in Figure 3(a) is particularly interesting. The
Figure 1 Examples of syllables retained after disabling
sound production on one side of the syrinx by occluding the
bronchus and sectioning the ipsilateral tracheosyringeal
nerve. (a–d) Syllables sung on right side, left side disabled.
(e– h) Syllables sung on left side, right side disabled. Number
identifying individual bird is in lower right corner of
each spectrogram.
Table 2 Effect of Plugging Left or Right Bronchus
and Ipsilateral Denervation of Syrinx on Subrepertoire
of Multinote Syllables
Bird
Side
Operated
Preoperative
Multinote
Repertoire*
Postoperative
Multinote
Repertoire*
1 Right 18/3 14/5
2 Right 17/2 20/4
3 Right 24/5 5/2
14 Right 29/0 1/0
Mean  SD: 22.0  5.6/
2.5  2.1
10.0  8.6/
2.7  2.2
4 Left 15/3 2/0
6 Left 11/0 4/0
9 Left 17/5 11/0
10 Left 9/3 4/0
Mean  SD: 13.0  3.7/
2.7  2.1
5.2  3.9/
0  0
*All multinote syllables/multinote syllables with repetition rate
 15 s
1. No preoperative multinote syllables sung faster than 13
s
1 were retained in the postoperative song.
384 Suthers et al.
first two notes are above 3 kHz and are retained after
the left bronchus was plugged, suggesting they were
also produced on the right side of the syrinx before
surgery. The third note starts at a lower frequency that
sweeps from about 1 to 5 kHz. It is probably produced
on the left side and its continued presence at a much
reduced intensity after the left bronchus was occluded
[Fig. 3(b), arrow] suggests that either enough air was
leaking past the bronchial plug to induce a low amplitude
vibration in the left syrinx or that mechanical
crosstalk from muscle activity on the plugged side
induced vibrations in the intact side of the syrinx.
Lateral Differences in Frequency Range. The frequency
range of postoperative song depends on which
side of the syrinx remains functional. Prior to denervating
the right side, almost a third of the syllables
extended to 6.2 kHz or higher, but after surgery none
of the syllables sung on the left side reached this
frequency and the number of syllables extending below
1.8 kHz increased. Forcing the bird to sing with
the right syrinx by disabling the left side had the
opposite effect. After this treatment, the proportion of
syllables extending above 6.2 kHz almost doubled
and there was a striking reduction in the number with
frequencies below 1.8 kHz compared to the preoperative
repertoire (Table 3; Fig. 1).
Syringeal lateralization of frequency range is also
apparent in the different frequencies of conserved and
semiconserved syllables sung on the left compared to
those on the right side. Disabling the right syrinx eliminated
high frequency notes (Fig. 2) whereas disabling
the left side eliminated low frequency notes (Fig. 3).
Syllables sung on the right side had most of their acoustic
energy above 3.5 kHz whereas those sung on the left
side had most of their energy below this frequency.
Figure 2 Examples of multinote syllables in preoperative repertoires that were partially conserved
after the right side was disabled. The left and right syrinx presumably contributed different notes to
original syllables. Preventing sound production on right side eliminates high frequency notes
without affecting low frequency notes. All postoperative notes (right column) were present in the
repertoire after the unilateral plug and after section of the ipsilateral tracheosyringeal nerve, except
(d), which was recorded only after the nerve was cut. See legend of Figure 1.
Song Production in Domestic Canaries 385
Mechanisms of Song Production in the
Intact Syrinx
The experiments with unilateral song production indicate
that both sides of the syrinx contribute to song
in domestic canaries. However, blocking and denervating
one side of the syrinx resulted in abnormal
respiratory dynamics and may affect syringeal biomechanics.
Furthermore, most of the repertoire changed
after surgery. In the following experiments we examine
the motor correlates of singing with a bilaterally
intact vocal system.
Figure 3 Examples of multinote syllables in preoperative repertoires that were partially conserved
after left side was disabled. Low frequency notes presumably sung on left side have disappeared but
high frequency notes from right side are unaffected. In (a) a faint rendition of the low frequency
note is still present (arrow) after the left bronchus was plugged, suggesting that a small amount of
air was leaking past the plug. This partially conserved syllable was not recorded after the ipsilateral
tracheosyringeal nerve was cut. The high notes of the other two syllables were present after the
bronchus was plugged and also after the nerve was cut. See legend of Figure 1.
Table 3 Effect of Left or Right Side Bronchus Plug and Syringeal Denervation on Sound Frequency*
Left Side Intact Right Side Intact
Preoperative Postoperative Preoperative Postoperative
Frequency bandwidth 3500 Hz 44 8 26 14
32% 6% 22% 13%
Maximum frequency 6200 Hz 44 0 18 34
32% 0% 15% 31%
Minimum frequency 1800 Hz 89 106 80 11
64% 84% 66% 10%
Total number of syllables n 138 127 121 110
*Number of syllables and percent of repertoire.
386 Suthers et al.
Song Lateralization in the Intact Syrinx. In order to
determine how the two sides of the intact syrinx
function, we monitored respiratory pressure and the
rate of airflow through the unobstructed left and right
bronchi in three males singing with their syringeal
innervation fully intact. During these experiments we
recorded a repertoire of 15, 23, and 21 different syllable
types from each of the three birds, respectively.
Domestic canaries differ from the waterslager
strain (Nottebohm and Nottebohm, 1976), in that both
sides of their syrinx make a substantial contribution to
song and there is no overwhelming unilateral dominance
of sound production (Fig. 4). Canary 9623 sang
10 unilaterally produced syllables, five on each side,
and five additional syllables in which each side contributed
sequentially. Canary 9823 sang one more
syllable on the right (43.5%) than on the left (39.1%),
with 17.4% of its repertoire receiving a contribution
from both sides. Canary 9996 produced slightly more
than half (52.4%) of its repertoire on the right side,
28.6% on the left side, with the remaining 19.0%
requiring both sides of the syrinx (Fig. 4). Whereas
the first two birds exhibited no lateral syringeal dominance
in song production, there was a moderate right
syringeal dominance in subject 9996.
Single note syllables [e.g., Figs. 5(b,c), 6(a,b)] and
also the individual notes within multinote syllables
[e.g., Figs. 5(a), 6(c), 7(a,b,c)] were produced unilaterally
by a partially adducted side of the syrinx while
the contralateral side was fully adducted and silent.
Vocalization was always accompanied by expiratory
airflow. Multinote syllables consisted of a sequence of
two or more nonoverlapping notes that were often
[e.g., Fig. 7(a,b,c)], but not always [Fig. 6(c)], generated
on opposite sides of the syrinx. The pattern of
syringeal lateralization for a given syllable type was
always the same each time it was produced. Twovoice
elements in which different sounds were produced
simultaneously on each side of the syrinx were
rare. Either side of the syrinx can produce strong
frequency modulation (FM) as well as nearly constant
frequency sound. Each side of the syrinx can also
produce syllables composed of more than one note
[e.g., Figs. 5(a) and 6(c)].
Vocal Registers of the Left and Right Intact Syrinx.
The lowest and highest fundamental frequency was determined
from the magnitude spectrum of each syllable
or the portion of it generated on each side of the syrinx
(Fig. 8). In all three birds, the lowest fundamental frequencies
are produced on the left side and the highest are
produced on the right, but with considerable overlap in
the midrange. The mean lowest fundamental frequency
for left side syllables was between 1.76 and 1.94 kHz
with some syllables extending below 1 kHz. The mean
lowest fundamental frequency of the right side syllables
ranged from 2.60 to 3.75 kHz. The mean highest fundamental
frequency was similarly shifted upward on the
right being 4.48 to 5.28 kHz compared to between 3.23
and 3.53 kHz on the left side. In syllables generated
bilaterally, there was a tendency to extend the leftgenerated
component to lower frequencies than were
present in unilaterally produced left syllables and to
increase the upper limit of the right-generated component,
compared to right-side syllables. These results
agree with those from birds with one side of their syrinx
silenced and indicate that an intact right syrinx is required
for producing high fundamental frequencies
whereas a functioning left side enhances the production
of low frequencies. The loss of motor control on either
side of the syrinx reduces the fundamental bandwidth of
the syllables.
Respiratory Pattern during Song. Each syllable is
accompanied by a stereotyped of respiratory pressure
and airflow. Except at very high syllable repetition rates,
most syllables are followed by a brief inspiration, a
minibreath, that maintains the respiratory volume and
permits the bird to sing long songs without running out
of air (Hartley and Suthers, 1989). In each bird, both
sides of the syrinx open for the intersyllable minibreath
in 68, 71, and 77% of the syllables sung by each of the
three birds, respectively. In almost all of the remaining
syllables (14 to 26% of each bird’s total repertoire) the
unilateral minibreath was on the right side, the remaining
5 to 9% being on the left side. Sometimes the sides
that participated in minibreaths varied irregularly during
a phrase between bilateral and right-side only inspirations
(Figs. 5, 6, and 7). The highest syllable repetition
Figure 4 Contribution from each side of the syrinx to
syllable production based on syringeal airflow in birds singing
with bilaterally intact vocal system. n  repertoire size.
Song Production in Domestic Canaries 387
rate sung with minibreaths by the three birds with bronchial
thermistors was 25 s
1 [Fig. 9(a)]. During this
syllable, the left syrinx was closed for the duration of the
phrase so both sound production and inspiration occurred
only on the right side. The right syrinx opens at
the peak of respiratory pressure, allowing a puff of
expiratory airflow to produce a syllable. It then closes
and immediately reopens for a minibreath when respiratory
pressure is negative. It is interesting that both
sides of the syrinx are closed as air sac pressure rises
immediately before phonation. This may facilitate a
more rapid increase in pressure and also allow time for
the right syrinx to be reconfigured for the next syllable.
Domestic canaries use a pattern of pulsatile expiration
at very high syllable repetition rates. The pulsatile
trill in Figure 9(b) is generated by the right syrinx and
has a syllable repetition rate of 23 s
1. Both its frequency
and amplitude are prominently modulated. Air
sac pressure is positive throughout the phrase and increases
during each syllable despite the fact that air is
flowing out through the right syrinx. This indicates active
participation of the expiratory muscles by increased
contraction during phonation. Each of the three amplitude
peaks in the syllable correspond to a small peak of
increased expiratory airflow, which is not reflected in the
air sac pressure and is most likely due to activity of the
right syringeal muscles. Perhaps to avoid interrupting the
song, the bird does not take a large inspiration before
beginning this phrase, which follows immediately after a
normal-size minibreath at the end of the preceding
phrase. Not until the end of the pulsatile phrase, which
terminates the song, is there a modest inspiration to
replace expended air. Although the syllable repetition
rate of the pulsatile phrase in Figure 9(b) is slightly
lower than that of the minibreath phrase in Figure 9(a),
the pulsatile syllables have a longer duration so the
intersyllable interval available for a minibreath is
shorter, about 22 ms compared to 36 ms in the phrase
using minibreaths.
DISCUSSION
Song Lateralization in Domestic Canaries
Direct measurements of subsyringeal pressure and
bronchial airflow in domestic canaries singing with a
Figure 5 Examples of syllables generated on the left side of the syrinx in birds singing with intact
vocal system. The first syllable is a bipartite complex syllable. Both parts of this syllable are
accompanied by relatively high rates of air flow through the left side. Although the right side is also
open briefly at the beginning of expiration, its declining and variable volume of airflow is not
reflected in the first note, to which it probably does not contribute. FR, airflow through right
bronchus; FL, airflow through left bronchus; P, pressure in cranial thoracic air sac; V, time waveform
of song. Horizontal lines indicate zero flow and ambient (zero) pressure. Inspiratory airflow is
shaded. L, sound from left side of syrinx. Syllable repetition rate is indicated at top of figure.
388 Suthers et al.
Figure 6 Examples of syllables generated on right side of syrinx. Second syllable is strongly
amplitude modulated. Last syllable contains two notes both produced on right side. R, sound from
right syrinx; for other abbreviations see legend of Figure 5.
Figure 7 Examples of syllables containing notes from each side of the syrinx. Bird changes side
of syrinx twice in first syllable. Expiratory airflow is switched from left side to right and back to left
to generate, respectively, an initial steep brief FM note, a gradual down sweep, and a terminal brief
steep FM note. In second and third syllables the first note is generated on the right side, followed
by a note on the left. See Figure 5 legend for abbreviations.
Song Production in Domestic Canaries 389
bilaterally intact syrinx clearly demonstrate that each
side of the vocal organ makes an important contribution
to the total song repertoire of this strain. In one
bird each side of the syrinx contributed an equal
number of syllables to the song repertoire, whereas in
the two other subjects there was a weak bias toward
the right side. All three birds frequently switched
sound production from one side to the other. Successive
notes of bilaterally generated syllables were usually
produced on different sides of the syrinx. Simultaneous
production of the same or different sounds on
both sides of the syrinx, resulting in two voice syllables,
was very rare or absent.
The results from birds singing with one side of
their syrinx silenced by a bronchial plug and hypoglossectomy
also indicate substantial contributions to
song from each side of the intact syrinx. Surgically
disabling either the left or right syrinx had little effect
on the repertoire size, showing that each side is capable
of producing a variety of syllables, but the
majority of postoperative syllables did not match
those present in preoperative song. Disabling one side
of the syrinx caused a marked decrease in the number
of multinote (i.e., complex) syllables in all but one
bird. This decrease was most pronounced after silencing
the left syrinx (Table 2). Some preoperative syllables
were retained, however, regardless of which
side of the syrinx was disabled, but this number was
greater when the left side of the syrinx remained
intact. Conserved syllables were presumably also
sung on the intact side of the syrinx before surgery.
Some of the two-note syllables in the preoperative
repertoires were represented after surgery by only one
of the notes, indicating that for these syllables each
note was originally produced on opposite sides. The
fact that the frequency range of the retained syllables
and notes corresponds to the vocal register of the
intact side supports the assumption that they were
produced on that side when the vocal system was
intact.
It is not clear why more preoperative syllables were
not retained after unilateral bronchus plugging and nerve
section or why so many new syllables were added. All
males in these experiments were in their second breeding
season and had stable song repertoires for at least 1
month before surgery. Perhaps the paralysis of one side
affected the biomechanics of the intact side, preventing
it from achieving the correct configuration or tension for
certain preoperative syllable types, which were thus
transformed into new syllables. In this case, however,
one might expect simple notes to be retained and complex
notes to be lost, because the former are presumably
easier to produce, but no such trend is evident. Conserved,
postoperative syllables include a wide range of
repetition rates and some unilaterally produced postoperative
syllables contained two notes. Postoperative syllables
occasionally included complex patterns of rising
and falling FM [e.g., Fig. 1(a,d)], prominent constant
frequency components, or steeply modulated FM.
It may be that the syllable retention is not determined
by the direct effects of peripheral intervention,
but rather by central changes induced by this intervention.
Halle et al. (2003) found in domestic canaries that
Figure 8 Range of fundamental frequencies produced on
each side of the syrinx. Vocal range of right side is higher
than that of left, but with substantial overlap between sides.
Bilateral sound production increases bandwidth. Mean
highest and lowest fundamental frequency (rectangle)  1
SD.
390 Suthers et al.
lesions in left HVC, a telencephalic song nucleus in the
efferent motor pathway, reduced the maximum syllable
repetition rate but right side lesions had no effect on this
parameter. Halle et al. suggest that some of these lateral
differences might reflect peripheral asymmetries that
may differentially affect the dynamics of air pressure
and airflow on the two sides of the syrinx, which in turn
might influence the gating of sound production.
Comparison with Waterslager Strain
The absence of a clear unilateral dominance in song
production by domestic canaries is in sharp contrast to
the prominent left syringeal dominance of the conspecific
waterslager strain and shows that lateralized song
production is not a universal trait of canaries. Nottebohm
and Nottebohm (1976) demonstrated that after
unilateral right tracheosyringeal nerve section, waterslager
canaries continued to sing 86 to 100% of their
preoperative song repertoire, whereas birds in which
the left tracheosyringeal nerve was cut sang only 0 to
26% of the preoperative repertoire. Lesions in the left
HVC had a much larger effect on song repertoire than
did lesions in the right HVC (Nottebohm, 1977).
The Nottebohms’ conclusion that song lateralization
is a central phenomenon was questioned by Mc-
Figure 9 Respiratory patterns at high syllable repetition rates. (a) Phrase sung at 25 syllables s
1
on right side with left syrinx closed. Both minibreaths and sound production are on right side. In
preceding phrase sound is switched from right to left and both sides participate in minibreaths. In
the following phrase sound is produced on left while right side is closed but opens during bilateral
minibreaths. R, right side; L, left side; B, both sides. Arrows indicate transitional syllables between
phrases. The second, and perhaps the first, of these transition syllables appear to have simultaneous
contributions from both sides. (b) Phrase sung at 23 syllables s
1 using pulsatile expiration. Air sac
pressure remains positive during entire phrase, which is produced on the right side with left side of
syrinx closed. Although repetition rate is lower than in minibreath phrase shown in upper panel, (a),
the silent interval available for an inspiration between syllables is shorter, presumably forcing the
bird to switch to pulsatile expiration.
Song Production in Domestic Canaries 391
Casland (1987), who argued, based on experiments in
which he plugged one or the other bronchus, that
differences in the effect of left versus right tracheosyringeal
nerve section on song may simply be due
the morphological differences in the syrinx that might
reduce the rate of airflow or strength of muscle contraction
on the right side of the syrinx, which has a
smaller diameter bronchus and 14% less muscle mass
than the left side (Luine et al., 1980). When Hartley
and Suthers (1990) attempted to replicate McCasland’s
bronchus plugging experiment, they obtained
results similar to those reported by the Nottebohms
after unilateral nerve section.
Recordings of respiratory pressure and airflow
through each side of the syrinx in waterslager canaries
singing with a bilaterally intact vocal system (Suthers,
1992, 1997, 1999) confirm that the strong left dominance
observed by Nottebohm is not an artifact of
disabling one side of the vocal organ. Even bilaterally
intact birds sing about 90% of their repertoire with the
left syrinx. The right syrinx is closed during these
syllables so that in the absence of airflow no sound is
produced. This situation is reversed during the minority
of syllables sung on the right side. Domestic
canaries and other songbirds studied use a similar
mechanism to determine which side of the syrinx
produces sound, but none are as strongly lateralized as
the waterslager. Waterslager canaries, like domestic
canaries, rarely deviate from this pattern to produce
sound simultaneously on both sides of the syrinx. The
lateralization of song production is determined by
both central and peripheral components (Goller and
Suthers, 1995).
Although the right syrinx contributes a relatively
small number of syllables to the waterslager repertoire,
it plays an important role in respiration during
song. For the majority of syllable types, the accompanying
minibreath is inhaled primarily or entirely
through the right syrinx. A likely advantage of this
arrangement is that it allows the left side of the syrinx
to remain in its partially adducted, phonatory position
throughout the phrase. In domestic canaries about
two-thirds of the syllables are accompanied by bilateral
minibreaths, but there is a strong preference for
the right side among the minority of syllables in
which the minibreath is unilateral.
The difference in song lateralization between waterslager
and domestic canaries is reflected in the
acoustic properties of their songs. Domestic canary
syllables often contain fundamental frequencies as
high as 6 or 7 kHz. The song of waterslager canaries,
on the other hand, is noted for its low frequency,
which is usually below 4 kHz. The inbred waterslager
strain has a severe hereditary sensorineural hearing
loss such that they are up to 40 dB less sensitive than
mixed breed canaries to frequencies above 2 kHz
(Gleich et al., 1994a,b, 2000; Wilkins et al., 2001). It
is possible that the strong left syringeal dominance of
this strain may be due to their reduced sensitivity to
the relatively high frequencies typically generated by
the right side of their syrinx.
Comparison with Other Species
Domestic canaries differ from other songbirds studied
(Suthers, 1999) in how the two sides of the syrinx
contribute to song. The simultaneous production of
unrelated sounds (two-voice syllables), so common in
brown thrashers and catbirds (Dumetella carolinesis)
(Suthers, 1990; Suthers et al., 1994), is very rare in
both domestic and waterslager canaries. Singing with
only one side of the syrinx at a time reduces the
volume of air needed to sing a syllable and therefore
the volume of the minibreath necessary to replenish
the air. This permits shorter minibreaths and may help
the bird achieve higher syllable repetition rates (Suthers
and Goller, 1997; Suthers, 1999).
Even in bilaterally generated domestic canary syllables,
the acoustic contribution from each side of the
syrinx is sequential rather than simultaneous. This is
also true for northern cardinals (Cardinalis cardinalis)
(Suthers, 1997) and brown-headed cowbirds (Molothrus
ater) (Allan and Suthers, 1994). Unlike canaries,
cowbirds alternate rapidly between sides of the
syrinx to generate note clusters within one respiratory
cycle. In cardinals the two sides of the syrinx cover
different frequency ranges and frequency modulated
sweeps from each side are often sequentially linked to
form one continuous broadband FM sweep. Domestic
canaries do not connect the sound from each side into
a continuous note.
In domestic canaries, the two sides of the syrinx
cover partially different frequency ranges. Although
the bandwidth of a canary’s repertoire extends from
about 1 to 6 or 7 kHz, the left syrinx usually does not
produce fundamental frequencies above about 3.6
kHz and the right syrinx usually does not extend
below about 2.5 kHz. This is consistent with the fact
that unilateral lesions in the sensorimotor song nucleus
HVC reduce syllable bandwidth by eliminating
either the highest or lowest frequencies, depending on
whether the lesion was on the right or left side,
respectively (Halle et al., 2003). A qualitatively similar
frequency lateralization has been observed in the
waterslager canary strain (Nottebohm and Nottebohm,
1976), zebra finch (Taeniopygia guttata) (Williams
et al., 1992), brown thrasher and grey catbird
(Suthers et al., 1994), brown-headed cowbird (Allan
392 Suthers et al.
and Suthers, 1994), northern cardinal (Suthers and
Goller, 1996), and northern mockingbird (Mimus
polyglottos) (Zollinger and Suthers, 2004). In all of
these species, the right side extends to higher frequencies
than the left and there is an overlapping midfrequency
range. A lateral specialization for different
fundamental frequencies thus appears to be a widespread
phenomenon among oscines that contributes to
their vocal versatility.
The physical or physiological basis for these different
vocal ranges is not known, but may involve
lateral asymmetries in the sound generating structures.
The presence of different left and right vocal
ranges makes it possible for the canary to increase
syllable bandwidth by including notes from each side
of the syrinx and demonstrates how the bipartite oscine
vocal organ can increase song diversity.
We thank Dr. Manfred Gahr for comments on an earlier
version of the manuscript, and Sandra Ronan, Ge´rard Clavelin,
and Jean-Pierre Lebrun (CLADIX-University Paris 10)
for technical assistance.
REFERENCES
Allan SE, Suthers RA. 1994. Lateralization and motor stereotypy
of song production in the brown-headed cowbird.
J Neurobiol 25:1154 –1166.
Gleich O, Dooling RJ, Manley GA. 1994a. Inner-ear abnormalities
and their functional consequences in Belgian
Waterslager canaries (Serinus canarius). Hearing Res 79:
123–136.
Gleich O, Dooling RJ, Ryals BM. 2000. Neither endocochlear
potential nor tegmentum vasculosum are affected
in hearing impaired Belgian Waterslager canaries. Hearing
Res 142:56–62.
Gleich O, Klump GM, Dooling RJ. 1994b. Hereditary sensorineural
hearing loss in a bird. Naturwissenschaften
81:320 –323.
Goller F, Suthers RA. 1995. Implications for lateralization
of bird song from unilateral gating of bilateral motor
patterns. Nature 373:63– 66.
G¨uttinger HR, Wolffgramm J, Thimm F. 1978. The relationship
between species specific song programs and individual
learning in song birds. Behaviour 65:241–262.
Halle F, Gahr M, Kreutzer M. 2003. Effects of unilateral
lesions of HVC on song patterns of male domesticated
canaries. J Neurobiol 56:303–314.
Hartley RS, Suthers RA. 1989. Airflow and pressure during
canary song: evidence for mini-breaths. J Comp Physiol
A 165:15–26.
Hartley RS, Suthers RA. 1990. Lateralization of syringeal
function during song production in the canary. J Neurobiol
21:1236 –1248.
Kreutzer M, Beme I, Vallet E, Kiosseva L. 1999. Social
stimulation modulates the use of the ’A’ phrase in male
canary songs. Behaviour 11:1–10.
Luine V, Nottebohm F, Harding C, McEwen BS. 1980.
Androgen affects cholinergic enzymes in syringeal motor
neurons and muscle. Brain Res 192:89 –107.
McCasland JS. 1987. Neuronal control of bird song production.
J Neurosci 7:23–39.
Mundinger PC. 1995. Behaviour-genetic analysis of canary
song: Inter-strain differences in sensory learning, and
epigenetic rules. Anim Behav 50:1491–1511.
Nottebohm F. 1977. Asymmetries in neural control of vocalization
in the canary. In: Harnad S, Doty RW, Goldstein L,
Jaynes J, Krauthamer G, editors. Lateralization in the nervous
system. New York: Academic Press, p 23–44.
Nottebohm F, Nottebohm ME. 1976. Left hypoglossal dominance
in the control of canary and white-crowned sparrow
song. J Comp Physiol 108:171–192.
Suthers RA. 1990. Contributions to birdsong from the left
and right sides of the intact syrinx. Nature 347:473– 477.
Suthers RA. 1992. Lateralization of sound production and
motor action on the left and right sides of the syrinx
during bird song. Proceedings 14th International Congress
on Acoustics: Vol 4, I1–5. Beijing, China.
Suthers RA. 1997. Peripheral control and lateralization of
birdsong. J Neurobiol 33:632– 652.
Suthers RA. 1999. The motor basis of vocal performance in
songbirds. In: Hauser M, Konishi M, editors. The Design
of Animal Communication. Cambridge, MA: MIT Press,
p 37–62.
Suthers RA, Goller F. 1996. Respiratory and syringeal dynamics
of song production in northern cardinals. In: Burrows
M, Matheson T, Newland P, Schuppe H, editors.
Nervous Systems and Behaviour. Proceedings of the 4th
International Congress of Neuroethology. Stuttgart:
Georg Thieme Verlag, p 333.
Suthers RA, Goller F. 1997. Motor correlates of vocal
diversity in songbirds. In: Nolan Jr V, Ketterson E,
Thompson CF, editors. Current Ornithology. Vol 14.
New York: Plenum Press, p 235–288.
Suthers RA, Goller F, Hartley RS. 1994. Motor dynamics of song
production by mimic thrushes. J Neurobiol 25:917–936.
Suthers RA, Goller F, Pytte C. 1999. The neuromuscular
control of birdsong. Phil Trans R Soc, Lond B 354:927–939.
Suthers RA, Vallet EM, Kreutzer M. 2004. The motor basis
of sexual signals in domestic canary song. Submitted.
Vallet E, Kreutzer M. 1995. Female canaries are sexually
responsive to special song phrases. Anim Behav 49:
1603–1610.
Wilkins HR, Presson JC, Popper AN, Ryals BM, Dooling
RJ. 2001. Hair cell death in a hearing-deficient canary. J
Assoc Res Otolaryngol 2:79–86.
Williams H, Crane LA, Hale TK, Esposito MA, Nottebohm
F. 1992. Right-side dominance for song control in the
Zebra Finch. J Neurobiol 23:1006 –1020.
Zollinger SA, Suthers RA. 2004. Motor mechanisms of a
vocal mimic: Implications for birdsong production. Proc
Roy Soc Lond B, to appear.

[Dr. Velev]

Никой ли не прочете статията или нивото е прекалено високо и неразбираемо , като се освободя малко ще и направя резюме .

[nightingale]

Аз я прочетох поне три пъти.
Да си призная с някои изрази се затрудних.
Пуснах я и през преводача но пък стана още по голямо мазало.
Ще ми е интересно да чуя резюме ,не на статията а на твоето виждане.
Зная че има какво да напишеш.
Ще чакам.

[Dr. Velev]

Ще го направя само заради твоя милост , Зомбираните не заслужават моето внимание и труд затова предпочитам на лична или в БНКЦК , където можеш да влизаш . Какво е казал Мойсей ..........

[nightingale]

Ще го направя само заради твоя милост , Зомбираните не заслужават моето внимание и труд затова предпочитам на лична или в БНКЦК , където можеш да влизаш . Какво е казал Мойсей ..........

Ще прочета трудът ти !
пп. Мойсей е казал - ''законът е всичко''

[Dr. Velev]

Казал е още ,че ще ги води ...докато не измре и последния неверник , чак тогаво са стигнали до обетованата земя .

[rules1]

супер яко мерси за инфото

Админ: До тук почти всичките ти мнения са спам.И този подпис ако заради него спамиш - да изчезне или аз ще го премахна

[paboev]

Казал е още ,че ще ги води ...докато не измре и последния неверник , чак тогаво са стигнали до обетованата земя .

Ти вече ставаш БОГ.Ти Бобо божи поведи ме в правилния път с песента на малиноата и и ми отвори третото око да я развера.

[Dr. Velev]

Приятелю ти си прогледнал и нямаш нужда да те водят.