J. exp. Bio/. (1980), 85, a39-»Si
With 6 figures
Printed in Great Britain
210
CONTROL OF SOUND PRODUCTION IN THE SYRINX
OF THE FOWL GALLUS GALLUS
BY JOHN BRACKENBURY
Department of Biology, University of Salford, Salford M5 \WT
(Received 15 June 1979)
SUMMARY
1. Changes in the configuration of the fowl syrinx during experimental
stimulation of the extrinsic syringeal muscles were assessed by monitoring
simultaneous changes in the airway resistance at a constant airflow rate.
2. Stimulation of the caudal part of the tracheolateralis muscle produced
a change away from the sound-producing configuration. The tympanum was
drawn craniad, the external tympaniform membranes were stretched and airway resistance fell as the syringeal lumen enlarged.
3. Stimulation of the sternotrachealis muscles produced a change towards
the sound-producing configuration. The tympanum was drawn caudad, the
membranes relaxed and airway resistance rose due to the constriction of the
syringeal lumen.
4. Tetanic stimulation of the cranial parts of both tracheolateralis and
tracheohyoideus produced a marked retraction of the larynx and rostral
part of the trachea.
5. The threshold levels of air-sac pressure and airflow rate necessary
to produce sound by passive ventilation of the respiratory system were
monitored. Passive sound could be abolished either by stimulating the
tracheolateralis muscle or by marginally increasing the tracheal resistance,
simulating glottal constriction.
6. Results are discussed in relation to current opinions on the importance
of active and passive factors during vocalization in birds. It is concluded that
the involvement of the extrinsic muscles may be necessary when producing
low volume sounds by relatively weak physical effort. Passive factors appear
to be more important during vigorous calling, such as crowing. In the latter
case the main function of the extrinsic muscles maybe to ensure the retraction
of the larynx and changes in shape of the anterior respiratory tract.
INTRODUCTION
Electromyographic studies by Youngren, Peek & Phillips (1974) and Gaunt &
Gaunt (1977) have shown that the extrinsic muscles of the fowl syrinx, the tracheolateralis (TL) and sternotrachealis (ST), are simultaneously active during a large
part of the crowing cycle. This finding casts some doubt on the theory originally
devised by Miskimen (1951), and since advocated by many authors, that it is the contraction of the ST that is responsible for bringing the syrinx into the sound-producing
configuration and that this action is opposed by the TL. The theory predicts that,
once the ST has brought about the initial displacement of the external tympaniform
240
J. BRACKENBURY
membranes into the syringeal lumen, further inward movement of the membranes
will occur as a result of the passive suction forces generated by the accelerating
airstream until a point is finally reached at which membrane vibration begins.
The observation that airway resistance increases markedly during vocalization has
been taken as evidence of the syringeal constriction that would be expected of the
original theory (Brackenbury, 1977, 1978 a, b) but the relative importance of active
and passive factors in this process is not known. On the other hand several workers
have demonstrated that spontaneous vocalization continues after de-activation of the
extrinsic syringeal muscles. The present experiments were designed to shed further
light on the interaction between muscular and aerodynamic forces during sound
production. The method employed was to monitor the changes in airway resistance
that result from stimulation of the muscles before and during artifical sound production and to relate these findings to alterations in the configuration of the syrinx.
METHODS
Studies were carried out on a total of 14 male and female chickens aged 12-17
weeks. Each was anaesthetized with a mixture of sodium pentobarbitone (30 mg/ml)
and ethyl carbamate (150 mg/ml) infused slowly into the wing vein, and prepared
for unidirectional ventilation as follows. The skin was reflected from the interclavicular area, the crop displaced to one side, the interclavicular air sac (ICS) cannulated
and a stream of warmed and humidified air led into the ICS and out of the beak.
Airflow rate was measured before entering the ICS by a Fleisch pneumotachograph
connected to a Grass PT5 manometer. A second manometer was used to monitor
ICS pressure. Both signals were displayed on a Grass Model 7 recorder.
Spontaneous respiratory movements were abolished by raising the airstream to a
level above the apnoeic threshold (approx. i-2l/min) and the skin incision was
carried forward along a mid-ventral line from the crop to the larynx. The descending
cervical branch of the left hypoglossal nerve was dissected free of the underlying TL
muscle for a length of 2-3 cm in the mid or caudal cervical level, severed and its
peripheral stump mounted on bipolar silver wire electrodes connected to a squarewave generator. Pulses of 5-7 V amplitude, and 0-3-0-5 ms duration, were delivered
at 2, 5, 10, 20, 50 and 100 Hz. The nerve—muscle preparation was kept moist with
Ringer at all times.
The ST was stimulated by paired, sharpened platinum-alloy electrodes inserted
directly into the muscles (one pair to each muscle) after the ICS had been completely
opened. In this case artificial ventilation was introduced via a mid-cervical tracheostomy, the direction of airflow was from the trachea to the lung air-sac system and
pressure changes were monitored on the tracheal side of the syrinx. This is the reverse
of the normal direction of airflow during vocalization and it is assumed that changes of
syringeal configuration due to muscle stimulation would exert qualitatively similar
effects on the measured flow resistance regardless ot flow direction, i.e. a constriction
of the syrinx would increase flow resistance and vice versa.
Some experiments involved raising the airflow rate to 3-5 1/min for brief periods
in order to elicit passive sound production. In these cases, in order to alleviate the
effects of excess C0 2 blow-off from the lung, artificial ventilation was discontinued
Sound production in the syrinx of the fowl
Hz
50
20
5
241
10 s
100
. i.... i.... i .
(a)
20
cm HjO
40 ml s"1
Hz
100
50
20'
5
100
20
Fig. 1. Changes in interclavicular air sac pressure (A) resulting from indirect stimulation of the
tracheolateralis muscles at the frequencies (Hz) shown at points (a) 3 cm and (6) :o cm cranial
to the air sac membrane. (B) Airflow rate. Airflow in the direction air sac to trachea. Stimulus
parameters: 7 V, 0-5 mi.
between procedures thus permitting the resumption of normal breathing and the
restoration of blood COj, levels.
RESULTS
Stimulation of the TL muscles
Direct and indirect stimulation of the caudal 8-10 cm of the TL resulted in a
caudo-cranial movement of the tympanum and a decrease in airway resistance (Fig. 1).
The latter was presumably caused by the tensing and drawing apart of the ETMs
and the consequent dilation of the syringeal lumen. No qualitative difference in
response was observed when the muscle was stimulated indirectly at points 10 cm
and 3 cm cranial to the ICS membrane. Since the descending cervical branch of the
hypoglossal innervates both the TL and ST muscles (Youngren et al. 1974), the
more caudal parts of this nerve might be expected to contain relatively greater numbers
J. BRACKENBURY
242
10s
I . I
Hz
I....I....I....I....I....I....I
5
10
20
50
100
I....I....I.
5
40 ml 5"
Hr
100
.50
20
5
100
20 mis-
Fig, a. Changes in tracheal pressure (A) resulting from direct stimulation of the sternotrachealis muscles at the frequencies (Hz) shown. (B) Airflow rate. Airflow in the direction
trachea to interclavicular air sac. Pulf ations of pressure and airflow are evident at subtetanic
stimulation frequencies in (a) at a flow rate of 40 ml/s but less evident in (6) at a flow rate of
ao ml/sec. Stimulus parameters: 7 V, 0-5 ms.
of motor fibres to the latter muscle. However, the present result suggests that if the
ST were indeed being activated at the same time as the TL, its strength of contraction
was never sufficient to reverse the action of the TL.
The contractile force of the TL, which could be measured by the total distance
moved by the tympanum and the resultant fall in airway resistance, was a function of
stimulation rate, rising from a negligible value at 5 Hz to a maximum at 100 Hz
Sound production in the syrinx of the fowl
243
Fig. 3. Changes interclavicular air sac pressure (A) and airflow rate (B) resulting from indirect
stimulation of the tracheolateralis muscles during artificial sound production. On the left
stepped increases in airflow rate are shown giving rise to graded increases in air-sac pressure.
Time bars indicate the periods of passive sound production (S). Sound production first began
at a point marked by the arrow when (A) and (B) were approximately 7 cm H,O and 40 ml/s
respectively. Periods between the time bars (s) indicate times of muscle stimulation. Stimulation in each case resulted in an immediate fall in pressure and the abolition of sound which
only resumed when stimulation ceased and air sac pressure began to rise again. Stimulus
parameters: 100 Hz, 5 V, 05 ms. Series of eight consecutive operations. The slope of the
zero line in (6) is due to amplifier drift.
(Fig. 1). Vibratory movement of the muscle was visibly evident at the lower stimulation frequencies, transforming into a fused response at ioo Hz. The resistance traces,
however, showed no signs of saw-tooth rise at subtetanic frequencies and summation
was always smooth. It appeared that the motion of the trachea was highly damped by
the viscoelastic drag of the extensible elements in the trachea and its confining
connective tissue sheaths.
Direct tetanic stimulation of the cranial part of the TL produced a marked retraction of the larynx and a telescoping of the rostral parts of the trachea.
Stimulation of the ST muscles
Direct bilateral stimulation of the paired ST muscles produced a graded rise in
airway resistance according to stimulation rate (Fig. 2). The response time of the
muscle was noticeably less than in the case of the TL and saw-tooth summation was
evident in the resistance trace at subtetanic stimulus frequencies. A fused response
appeared to occur at 50 Hz but overall contraction was greater at 100 Hz. The lower
response time of the ST as compared to the TL may be due to differences in muscle
loading rather than intrinsic differences in contractile properties. Since the ST acts
upon only the relatively inextensible posterior parts of the trachea and the tympanum,
its loading is relatively discrete and stiff, and its contraction markedly isometric. In
contrast the trachea presents a comparatively extensible loading to the TL and the
contraction of the latter is markedly isotonic. I am not aware of any histological
differences between the TL and ST muscles but clearly information on this matter
be of value.
244
J. BRACKENBURY
Sound
Sound
(a)
Sound i
(6)
10 s
cmH,0
.T
1O
Fig. 4. Changes in interclavicular air-sac pressure (A) and airflow rate (B) before and during
artificial sound production. Time bars indicate the periods of sound production. At points
marked by the small and large arrows the tympanum was slowly pushed towards and away from
the petsulus respectively. In (a) the beginning of the sound bars indicate the threshold pressures
andflowsat which sound began in two successive manipulations. In (6) thefirstmanipulation
was successful in eliciting sound but the following manipulations produced excessive compression of the syrinx and sound did not occur. Series of two operations in (a) and seven operations
in (6).
Stimulation of the tracheohyoideus (TH)
Direct stimulation of the cranial half of the TH produced a qualitatively similar
effect to that of the TL, namely laryngeal retraction and tracheal shortening.
Experimental sound production and abolition
The syrinx can produce sound passively provided the instantaneous airflow rate
and air pressure within the lung air-sac system exceed certain threshold values. The
minimal values observed in these experiments were approximately 40 ml/s and
5 cm HaO (5 x io 2 N/m a ) respectively, although in several animals larger values were
necessary. Passive sound production could be abolished immediately by tetanic
stimulation of the TL muscles (Fig. 3).
An alternative method for producing sound without increasing flow rate is to push
the tympanum manually towards the pessulus, the cartilage lying at the opposite end
Sound production in the syrinx of the fowl
Sound
Sound
245
Sound
i....i....I....i.
8 mis
Fig. 5. Change* in interclavicular air sac pressure (A) and airflow rate (B) during artificial
sound production and its abolition. Time bars indicate the periods of sound production.
Sound wag begun by pushing the tympanum caudally and fixing it in the effective position. At
the arrowed points the screw-clip on the tracheostomy was slowly closed. A few seconds
later sound production fell dramatically and ceased as the air-sac pressure and airflow began to
rise and fall respectively. Sound production was resumed when the aerodynamic parameters
returned to their previous levels as the screw-clip was re-opened. Two consecutive operations
shown.
of the syrinx (Fig. 6). This simulates the action of the ST muscle and produces an
initial rise in airway resistance followed by a gradual rise in air sac pressure as the
lung air sac system begins to accumulate air against the raised downstream pressure.
At the same time the increased load on the supply stream may cause it to fall slightly
but a point is eventually reached at which both ICS pressure and airflow rate are in
excess of threshold values and the ETMs are triggered into vibration (Fig. 4a). The
mechanism is sensitive to manipulation and over-displacement of the tympanum
distorts the syrinx to such an extent that ICS pressure and airflow may rise and fall
precipitously without achieving even momentarily a combination of values suitable
for sound production (Fig. 46).
The latter is an example of gross impairment of the sound-production mechanism,
but a situation can also be demonstrated in which marginal increases in pressure and
decreases in airflow rate will lead to the abolition of existing sound. Fig. 5 shows the
results of an experiment on a tracheostomised individual receiving unidirectional
ventilation into the ICS. First, sound was induced by displacing the tympanum and
fixing it in the effective position. Next, the resistance of the trachea was altered by
tightening a screw-clip attached to the tracheostomy tube. Sound volume fell rapidly
when a point was reached at which ICS pressure and airflow began to rise and fall
almost imperceptibly; further tightening of the screw-clip produced measurable
changes in the aerodynamic parameters and sound was abolished. Sound was restored
by reopening the screw-clip and returning pressure and flow to their previous levels.
These experiments illustrate the necessity of achieving adequate simultaneous levels
246
J. BRACKENBURY
of ICS pressure and airflow in order to excite the ETMs. If the increase in ICS
pressure is achieved only at the expense of an excessive decline in air flow, either by
over-compression of the longitudinal axis of the syrinx or by an increase in downstream
resistance as might result from active glottal constriction, the aero-mechanical coupling
between the airstream and the ETMs fails to occur.
DISCUSSION
Note on muscle terminology
Workers interested in vocal mechanisms have classified the tracheal muscles as
extrinsic muscles of the syrinx; others (McLelland, 1965; White, 1968: White &
Chubb, 1968; King, 1975) have referred to them as the caudal extrinsic muscles of
the larynx. The latter workers, moreover, regard the cranial attachment of the ST
as being the larynx, not the trachea, and hence they call it the sternolaryngeus. They
regard the ST and TL as forming a single muscle over the cranial length of the
trachea, the sternotracheolaryngeus. However, since Youngren et al. (1974) and
Gaunt and Gaunt (1977) have demonstrated the separate functional identity of these
muscles, their terminology will be retained in the present paper in order to avoid
confusion. It remains true, nevertheless, that the TL should properly be referred to
as the tracheolaryngeus since it inserts cranially on to the larynx whilst the TH should
be referred to as the sternolaryngeus since it attaches caudally on the sternum and
cranially on the larynx.
Functions of the ST and TL muscles
Present results confirm that contraction of the ST leads to a shortening of the distance between the tympanum and the pessulus, a slackening of the ETMs and partial
occlusion of the syringeal lumen (Fig. 2). They thus lend support to the view expressed
by many workers that one of the important functions of the ST is to bring about the
initial yielding of the ETMs that will ultimately lead to their becoming coupled in an
exchange of energy with the airstream (Miskimen, 1951; Gross, 1964a; Chamberlain,
Gross, Cornwell & Mosby, 1968; Greenewalt, 1968; Gaunt, Gaunt & Hector, 1976;
Gaunt & Gaunt, 1977; Youngren et al. 1974; Brackenbury, 1978a, b). The ST could
achieve these effects directly at its point of insertion by pulling the tympanum caudad,
or indirectly by tensing the syringeal ligament which then pulls the pessulus forward,
as described by Youngren et al and Gaunt & Gaunt. Whatever the precise mechanism,
the coupling between the airstream and the ETMs can occur only if ICS pressures
and airflow rates of sufficient magnitude exist at the time of muscular contraction.
At subthreshold flow rates, such as those employed in Fig. 2, partial invasion by the
ETMs takes place, as reflected by a rise in airway resistance, but the positive feedback
of energy from the air to the elastic membranes is insufficient to trigger their oscillation.
The TL cannot be assigned a single role since both its extreme points of attachment, the caudal end of the trachea and the larynx, are capable of acting as either
origin or insertion depending on their degree of stabilization by other muscles. Thus,
if its posterior point were anchored by the ST, and if the rostral extrinsic laryngeal
muscles were simultaneously relaxed, contraction of the TL would produce a retraction of the larynx. However, it is generally accepted that contraction of the more
Sound production in the syrinx of the fowl
247
ST
ETM
PB
Fig. 6. Semi-diagrammatic interpretation of muscular movements during crowing in the fowl.
Full arrows represent contraction, dashed arrows relaxation or stretch. Contraction of the cranial
parts of the tracheolateralis (TL) and tracheohyoideus (TH) muscles, together with simultaneous relaxation of the rostral extrinsic laryngeal muscles (REL) and passive stretch of the
arytenoglossal ligaments (AGL), produces a retraction of the larynx (L) and telescoping of the
rostral segments of the trachea. Simultaneously the activated stemotrachealis (ST) undergoes active stretch by the T L , the tympanum (T) is drawn craniad with respect to the pessulus
(P) and primary bronchi (PB) and the external tympaniform membranes (ETM) are stretched.
The tension (t) produced in the E T M S and S T muscle cannot exceed that produced in the
REL and AGL. ICS: boundary of the interclavicular air sac. The T H is shown displaced from
the mid-line where it normally runs alongside the trachea.
caudal part of the TL, by exerting a caudorostral force on the tympanum, tends to
remove the syrinx from the vocal configuration. This is borne out by the measured
decrease in syringeal resistance shown in Fig. 1 and the abolition of pre-existing sound
shown in Fig. 3. The apparent contradiction in the finding by Youngren et al. (1974)
and Gaunt and Gaunt (1977) that both the TL and ST may be active during vocalization can be resolved by assuming, along with these authors, that the muscles are able,
by finely graded opposition of action, to exercise a greater degree of control over the
axial length of the syrinx and thus over the effectiveness of the aeromechanical
•mpling process in any given conditions.
248
J. BRACKENBURY
Gaunt & Gaunt (1977) have analysed the way in which such co-ordinated muscular
activity may explain the production of certain types of high-pitched wailing sounds
which occur in chickens. Simultaneous recordings of tracheal pressure and muscle
activity suggest that airflow is relatively unimpeded and that the ETMs are being held
taut by strong contraction of the TL. Gaunt and Gaunt propose that contraction of
the TL, by stabilizing its joint insertion with the ST also permits the latter to exert
sufficient tension on the syringeal ligament to draw the pessulus forward and relax the
posterior margin of the membranes. Only a very slight movement of the pessulus
appears to be necessary for sound production to occur in these circumstances.
Youngren et al. (1974) concluded that, although it had a role during vocalization,
the TL was primarily an accessory respiratory muscle since, unlike the ST, it was also
active during normal breathing. They proposed that its chief function was to maintain
the patency of the airway against adverse positive pressures in the ICS although of
course this was also compatible with a steering role for the syrinx during vocalization.
Gaunt & Gaunt (1977) expressed reservations on the normal respiratory function
of the TL but agreed that it might prevent collapse of the ETMs during rapid,
dyspnoeic inspirations. The present author can confirm the presence of strong inspiratory activity in the TL during stressed breathing in anaesthetized birds. Since
resting respiratory pressures never exceed + 1-2 cm H2O (1-2 x io e N m~2) there
would seem little danger of ETM collapse in normal conditions. Moreover, owing to
the existence of a low-resistance pathway from the ICS to the primary bronchi,
via the third ventrobronchus of the lung (King, 1975), there is every chance that
even large hydrostatic pressures in the ICS will be equalized across the ETMs, so long
as concomitant airflow rates are small. When airflow rates are concomitantly large,
local kinetic forces in the syrinx will of course tend to draw in the membranes during
either expiration or inspiration.
White (1968) recognized the importance of the TL and TH (her 'caudal extrinsic
laryngeal muscles') in bringing about a gross retraction of the larynx during crowing
in cockerels. Powerful retraction of the larynx in response to direct stimulation of
these muscles has been reported in the present study and also by Gaunt & Gaunt
(1977). The function of laryngeal retraction during vocalization is not clear but it is
possible that the resultant decrease in overall tracheal length and tracheal resistance
might influence the efficiency of the syringeal mechanism. Fig. 5 demonstrates the
sensitivity of the mechanism to alterations in downstream pressure and resistance;
any means that led to a reduction in the potentially large tracheal pressures resulting
from the dramatically increased airflows during vocalization (Brackenbury, 1977)
would be advantageous to sound production.
White (1968) and Gaunt & Gaunt (1977) have suggested another possible function
for laryngeal retraction: to influence sound quality by altering the shape of the pharyngeal cavity. Audiospectrograms of crowing in adult chickens show it to be very rich in
overtones (Collias & Joos, 1953; Konishi, 1963; Wood-Gush, 1971) but these seem
to be governed by tracheal length and ETM tension (Harris, Gross & Robeson, 1968;
Abs, 1969; Gaunt & Wells, 1973; Lockner & Murrish, 1975). The characteristic
tonal structure of the crow appears only after the voice has broken (Marler, Kreis &
Willis, 1962) and further studies on voice-break in relation to the development of full
activity in the tracheal muscles would help clarify this problem.
Sound production in the syrinx of the fowl
249
Interrelationships of active and passive factors during vocalization
Several workers have shown that experimental de-activation of the vocal muscles
will not silence birds (Miskimen, 1951; Youngren et al. 1974; Smith, 1977; Brackenbury, 19786) and Gross (19746) was led to the conclusion that it is almost impossible
to abolish sound production by any means short of serious interference with the
respiratory process itself. Simply by the expedient of raising their expiratory effort,
operated animals appear to be able to compensate for the lack of muscular involvement.
Normally, contraction of the ST facilitates the coupling between airflow and the
ETMs; the extra effort in operated animals suffices to bring the relaxed membranes
to the yield point and thus onto the force cascade leading to membrane oscillation.
Use of the vocal muscles economizes on effort since it allows triggering of the
audiogenerator at relatively low air-sac pressures and airflow rates; indeed they may
be indispensable for the production of low volume sounds that require minimal
physical effort. In contrast, during crowing the normal muscular controls in favour
of economy of effort appear to be sacrificed in order to obtain maximum sound output
at maximum possible airflow rates. From their comparison of audio-spectrograms of
normal crowing and of sounds elicited from excised syrinxes Harris et al. (1968) deduced that the ETMs must be held in a position of near maximal stretch throughout
the crowing cycle. This would imply that the TL undergoes powerful contraction
only weakly opposed by the much smaller ST muscle. The latter may serve partly as a
ligamentar muscle which, by means of undergoing limited 'active stretch' by the TL,
serves to provide a relatively stable anchorage from which the much larger muscle can
exert maximal retractile force on the larynx. Moreover, the same anchorage may also
allow the ST to stretch the syringeal ligament and relax the ETMs as described by
Gaunt and Gaunt in their analysis of the wail in chickens.
At the same time insurance against excessive tensile pull on the syrinx and ST
muscles is procured by a novel means. For, as White (1968) reasoned, retraction of
the larynx must be accompanied by relaxation of the rostral extrinsic laryngeal muscles
and stretch of the aryteno-glossal ligaments, both of which connect the larynx to the
hyoid. This means that the tension generated by the TL is relayed to elastic elements
at the rostral end as well as at the caudal end (Fig. 6). Physical considerations dictate
that the tension in the ST and syringeal membranes cannot exceed that in the rostral
elastic elements. Both sets of elements also serve to limit the contractile force generated
by the TL by allowing it to contract in an isotonic, as opposed to an isometric, manner.
They are assisted in this task by the series of elastic elements within the trachea itself.
The elastic loading of the TL by these various elements explains the rather sluggish
contractile response of the muscles to electrical stimulation (Fig. 1).
Various circumstances accompanying crowing, such as gross laryngeal retraction,
near maximal stretch of the ETMs and incomparably high expiratory flow rates,
suggest an effort on the part of the bird to achieve the maximum possible unimpeded
airflow. The advantages may be twofold: first, since the total fluid power available
for driving the membranes is proportional to airflow2 (Brackenbury, 1979a) it pays
double dividends to minimise flow obstruction; second, it is possible that very high
flow rates may permit the exploitation of a novel form of convective sound amplifica-
250
J. BRACKENBURY
tion which avoids the need to produce unduly large membrane vibration amplitudes
and consequent overloading of the membranes (Brackenbury, 19796).
Airflow resistance during vocalization
The observed increase in airway resistance during crowing has previously been
ascribed mainly to the partial occlusion of the syringeal lumen by the ETMs but also
partly to purely aerodynamic forces that cause the pressure/flow relationship to rise
non-linearly at higher flow rates (Brackenbury, 19786). Amongst these forces, those
due to turbulent airflow through the syrinx seem the strongest candidate. If, as a
result of the contraction of the TL muscle, the syringeal lumen is not occluded to the
extent previously envisaged, a greater attribution must be made to this turbulent
source of resistance.
Neural control of muscles of the anterior respiratory tract
The ST, TL and TH are hypobranchial muscles derived from ventral extensions of
the post-occipital somites of the embryo and thus share a common innervation by the
hypoglossal nerve, with the intrinsic muscles of the hyoid and tongue and the rostral
extrinsic muscles of the larynx (Weichert, 1970). Their primitive functional associations are therefore with acts involving adjustment to the shape of the anterior respiratory tract, such as deglutition, coughing and, in appropriate circumstances, respiration. The association between respiratory movements and tracheal muscle activity
is probably very loose during normal respiration but it becomes more evident during
dyspnea and thermal polypnea. The fluttering movements of the throat (gular flutter)
of many birds during panting (Calder & Schmidt-Nielsen, 1968) involve the coordinated activity of the hyoid and extrinsic laryngeal muscles, including the TL and
TH. It can be demonstrated that the cranial motor nuclei of the hypoglossal, as well
as the vagus and glossopharyngeal nerves, receive dual control by the panting centre
and the respiratory centre (Brackenbury, 1978c). The hypoglossal nuclei, and the
muscles that they serve, are thus amenable to control by at least two other central
areas in addition to the vocal centres of the mid-brain (Potash, 1970; Peek & Phillips,
1971; Phillips, Youngren & Peek, 1972). Only in a limited sense, therefore, can the
extrinsic syringeal muscles be regarded as ' vocal' muscles. Truly vocal muscles exist
in the syrinx of passerine birds but virtually nothing is known about their detailed
innervation and control.
Voluntary inhibition of sound production
Natural physiological situations occur that involve the production of aerodynamic
forces in excess of the threshold for passive sound production but for purposes
entirely unrelated to vocalization, such as defaecation, preening and coughing. From
the experimental situation illustrated in Fig. 5 it can be inferred that an effective
device for reducing spurious sound production is active constriction of the glottis, for
this elevates tracheal resistance and impairs the syringeal mechanism and this is
precisely what appears to occur during defaecation and vigorous preening (Brackenbury
19786).
This work was supported by the Science Research Council.
Sound production in the syrinx of the fowl
251
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