J. exp. Bio/. (1980), 85, a39-»Si 2 1 0With 6 figures

Printed in Great Britain

CONTROL OF SOUND PRODUCTION IN THE SYRINXOF THE FOWL GALLUS GALLUS

BY JOHN BRACKENBURYDepartment of Biology, University of Salford, Salford M5 \WT

(Received 15 June 1979)

SUMMARY

1. Changes in the configuration of the fowl syrinx during experimentalstimulation of the extrinsic syringeal muscles were assessed by monitoringsimultaneous changes in the airway resistance at a constant airflow rate.

2. Stimulation of the caudal part of the tracheolateralis muscle produceda change away from the sound-producing configuration. The tympanum wasdrawn craniad, the external tympaniform membranes were stretched and air-way resistance fell as the syringeal lumen enlarged.

3. Stimulation of the sternotrachealis muscles produced a change towardsthe sound-producing configuration. The tympanum was drawn caudad, themembranes relaxed and airway resistance rose due to the constriction of thesyringeal lumen.

4. Tetanic stimulation of the cranial parts of both tracheolateralis andtracheohyoideus produced a marked retraction of the larynx and rostralpart of the trachea.

5. The threshold levels of air-sac pressure and airflow rate necessaryto produce sound by passive ventilation of the respiratory system weremonitored. Passive sound could be abolished either by stimulating thetracheolateralis muscle or by marginally increasing the tracheal resistance,simulating glottal constriction.

6. Results are discussed in relation to current opinions on the importanceof active and passive factors during vocalization in birds. It is concluded thatthe involvement of the extrinsic muscles may be necessary when producinglow volume sounds by relatively weak physical effort. Passive factors appearto be more important during vigorous calling, such as crowing. In the lattercase the main function of the extrinsic muscles maybe to ensure the retractionof 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 tracheo-lateralis (TL) and sternotrachealis (ST), are simultaneously active during a largepart of the crowing cycle. This finding casts some doubt on the theory originallydevised by Miskimen (1951), and since advocated by many authors, that it is the con-traction of the ST that is responsible for bringing the syrinx into the sound-producingconfiguration 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 membraneswill occur as a result of the passive suction forces generated by the acceleratingairstream until a point is finally reached at which membrane vibration begins.

The observation that airway resistance increases markedly during vocalization hasbeen taken as evidence of the syringeal constriction that would be expected of theoriginal theory (Brackenbury, 1977, 1978 a, b) but the relative importance of activeand passive factors in this process is not known. On the other hand several workershave demonstrated that spontaneous vocalization continues after de-activation of theextrinsic syringeal muscles. The present experiments were designed to shed furtherlight on the interaction between muscular and aerodynamic forces during soundproduction. The method employed was to monitor the changes in airway resistancethat result from stimulation of the muscles before and during artifical sound pro-duction 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 12-17weeks. 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 preparedfor unidirectional ventilation as follows. The skin was reflected from the interclavi-cular area, the crop displaced to one side, the interclavicular air sac (ICS) cannulatedand 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 pneumotachographconnected to a Grass PT5 manometer. A second manometer was used to monitorICS pressure. Both signals were displayed on a Grass Model 7 recorder.

Spontaneous respiratory movements were abolished by raising the airstream to alevel above the apnoeic threshold (approx. i-2l/min) and the skin incision wascarried forward along a mid-ventral line from the crop to the larynx. The descendingcervical branch of the left hypoglossal nerve was dissected free of the underlying TLmuscle for a length of 2-3 cm in the mid or caudal cervical level, severed and itsperipheral stump mounted on bipolar silver wire electrodes connected to a square-wave generator. Pulses of 5-7 V amplitude, and 0-3-0-5 ms duration, were deliveredat 2, 5, 10, 20, 50 and 100 Hz. The nerve—muscle preparation was kept moist withRinger at all times.

The ST was stimulated by paired, sharpened platinum-alloy electrodes inserteddirectly into the muscles (one pair to each muscle) after the ICS had been completelyopened. In this case artificial ventilation was introduced via a mid-cervical tracheos-tomy, the direction of airflow was from the trachea to the lung air-sac system andpressure changes were monitored on the tracheal side of the syrinx. This is the reverseof the normal direction of airflow during vocalization and it is assumed that changes ofsyringeal configuration due to muscle stimulation would exert qualitatively similareffects on the measured flow resistance regardless ot flow direction, i.e. a constrictionof the syrinx would increase flow resistance and vice versa.

Some experiments involved raising the airflow rate to 3-5 1/min for brief periodsin order to elicit passive sound production. In these cases, in order to alleviate theeffects of excess C02 blow-off from the lung, artificial ventilation was discontinued

Sound production in the syrinx of the fowl

Hz 5 20 50 100 10 s

. i . . . . i . . . . i .

241

(a) 20cm 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 thetracheolateralis muscles at the frequencies (Hz) shown at points (a) 3 cm and (6) :o cm cranialto the air sac membrane. (B) Airflow rate. Airflow in the direction air sac to trachea. Stimulusparameters: 7 V, 0-5 mi.

between procedures thus permitting the resumption of normal breathing and therestoration 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 acaudo-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 ETMsand the consequent dilation of the syringeal lumen. No qualitative difference inresponse was observed when the muscle was stimulated indirectly at points 10 cmand 3 cm cranial to the ICS membrane. Since the descending cervical branch of thehypoglossal innervates both the TL and ST muscles (Youngren et al. 1974), themore caudal parts of this nerve might be expected to contain relatively greater numbers

242 J. BRACKENBURY

10s

I . I I . . . . I . . . . I . . . . I . . . . I . . . . I . . . . I I . . . . I . . . . I .

Hz 5 10 20 50 100 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 sterno-trachealis muscles at the frequencies (Hz) shown. (B) Airflow rate. Airflow in the directiontrachea to interclavicular air sac. Pulf ations of pressure and airflow are evident at subtetanicstimulation frequencies in (a) at a flow rate of 40 ml/s but less evident in (6) at a flow rate ofao ml/sec. Stimulus parameters: 7 V, 0-5 ms.

of motor fibres to the latter muscle. However, the present result suggests that if theST were indeed being activated at the same time as the TL, its strength of contractionwas never sufficient to reverse the action of the TL.

The contractile force of the TL, which could be measured by the total distancemoved by the tympanum and the resultant fall in airway resistance, was a function ofstimulation 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 indirectstimulation of the tracheolateralis muscles during artificial sound production. On the leftstepped 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 beganat a point marked by the arrow when (A) and (B) were approximately 7 cm H,O and 40 ml/srespectively. Periods between the time bars (s) indicate times of muscle stimulation. Stimula-tion in each case resulted in an immediate fall in pressure and the abolition of sound whichonly resumed when stimulation ceased and air sac pressure began to rise again. Stimulusparameters: 100 Hz, 5 V, 05 ms. Series of eight consecutive operations. The slope of thezero line in (6) is due to amplifier drift.

(Fig. 1). Vibratory movement of the muscle was visibly evident at the lower stimula-tion frequencies, transforming into a fused response at ioo Hz. The resistance traces,however, showed no signs of saw-tooth rise at subtetanic frequencies and summationwas always smooth. It appeared that the motion of the trachea was highly damped bythe viscoelastic drag of the extensible elements in the trachea and its confiningconnective tissue sheaths.

Direct tetanic stimulation of the cranial part of the TL produced a marked retrac-tion 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 inairway resistance according to stimulation rate (Fig. 2). The response time of themuscle was noticeably less than in the case of the TL and saw-tooth summation wasevident in the resistance trace at subtetanic stimulus frequencies. A fused responseappeared to occur at 50 Hz but overall contraction was greater at 100 Hz. The lowerresponse time of the ST as compared to the TL may be due to differences in muscleloading rather than intrinsic differences in contractile properties. Since the ST actsupon only the relatively inextensible posterior parts of the trachea and the tympanum,its loading is relatively discrete and stiff, and its contraction markedly isometric. Incontrast the trachea presents a comparatively extensible loading to the TL and thecontraction of the latter is markedly isotonic. I am not aware of any histologicaldifferences between the TL and ST muscles but clearly information on this matter

be of value.

244 J. BRACKENBURY

Sound Sound

(a)

Sound i 10 s

cmH,0

(6) 1O.T

Fig. 4. Changes in interclavicular air-sac pressure (A) and airflow rate (B) before and duringartificial sound production. Time bars indicate the periods of sound production. At pointsmarked by the small and large arrows the tympanum was slowly pushed towards and away fromthe petsulus respectively. In (a) the beginning of the sound bars indicate the threshold pressuresand flows at which sound began in two successive manipulations. In (6) the first manipulationwas successful in eliciting sound but the following manipulations produced excessive compres-sion of the syrinx and sound did not occur. Series of two operations in (a) and seven operationsin (6).

Stimulation of the tracheohyoideus (TH)

Direct stimulation of the cranial half of the TH produced a qualitatively similareffect 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 rateand air pressure within the lung air-sac system exceed certain threshold values. Theminimal values observed in these experiments were approximately 40 ml/s and5 cm HaO (5 x io2 N/ma) respectively, although in several animals larger values werenecessary. Passive sound production could be abolished immediately by tetanicstimulation of the TL muscles (Fig. 3).

An alternative method for producing sound without increasing flow rate is to pushthe tympanum manually towards the pessulus, the cartilage lying at the opposite end

Sound production in the syrinx of the fowl 245

Sound Sound Sound

i . . . . i . . . . I . . . . i .

8 mis

Fig. 5. Change* in interclavicular air sac pressure (A) and airflow rate (B) during artificialsound 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. Atthe arrowed points the screw-clip on the tracheostomy was slowly closed. A few secondslater sound production fell dramatically and ceased as the air-sac pressure and airflow began torise and fall respectively. Sound production was resumed when the aerodynamic parametersreturned to their previous levels as the screw-clip was re-opened. Two consecutive operationsshown.

of the syrinx (Fig. 6). This simulates the action of the ST muscle and produces aninitial rise in airway resistance followed by a gradual rise in air sac pressure as thelung 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 slightlybut a point is eventually reached at which both ICS pressure and airflow rate are inexcess of threshold values and the ETMs are triggered into vibration (Fig. 4a). Themechanism is sensitive to manipulation and over-displacement of the tympanumdistorts the syrinx to such an extent that ICS pressure and airflow may rise and fallprecipitously without achieving even momentarily a combination of values suitablefor 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 anddecreases in airflow rate will lead to the abolition of existing sound. Fig. 5 shows theresults of an experiment on a tracheostomised individual receiving unidirectionalventilation into the ICS. First, sound was induced by displacing the tympanum andfixing it in the effective position. Next, the resistance of the trachea was altered bytightening a screw-clip attached to the tracheostomy tube. Sound volume fell rapidlywhen a point was reached at which ICS pressure and airflow began to rise and fallalmost imperceptibly; further tightening of the screw-clip produced measurablechanges in the aerodynamic parameters and sound was abolished. Sound was restoredby 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 ICSpressure is achieved only at the expense of an excessive decline in air flow, either byover-compression of the longitudinal axis of the syrinx or by an increase in downstreamresistance as might result from active glottal constriction, the aero-mechanical couplingbetween the airstream and the ETMs fails to occur.

DISCUSSION

Note on muscle terminology

Workers interested in vocal mechanisms have classified the tracheal muscles asextrinsic muscles of the syrinx; others (McLelland, 1965; White, 1968: White &Chubb, 1968; King, 1975) have referred to them as the caudal extrinsic muscles ofthe larynx. The latter workers, moreover, regard the cranial attachment of the STas being the larynx, not the trachea, and hence they call it the sternolaryngeus. Theyregard the ST and TL as forming a single muscle over the cranial length of thetrachea, the sternotracheolaryngeus. However, since Youngren et al. (1974) andGaunt and Gaunt (1977) have demonstrated the separate functional identity of thesemuscles, their terminology will be retained in the present paper in order to avoidconfusion. It remains true, nevertheless, that the TL should properly be referred toas the tracheolaryngeus since it inserts cranially on to the larynx whilst the TH shouldbe referred to as the sternolaryngeus since it attaches caudally on the sternum andcranially on the larynx.

Functions of the ST and TL muscles

Present results confirm that contraction of the ST leads to a shortening of the dis-tance between the tympanum and the pessulus, a slackening of the ETMs and partialocclusion of the syringeal lumen (Fig. 2). They thus lend support to the view expressedby many workers that one of the important functions of the ST is to bring about theinitial yielding of the ETMs that will ultimately lead to their becoming coupled in anexchange 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 couldachieve 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 pressuresand 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 theETMs takes place, as reflected by a rise in airway resistance, but the positive feedbackof energy from the air to the elastic membranes is insufficient to trigger their oscilla-tion.

The TL cannot be assigned a single role since both its extreme points of attach-ment, the caudal end of the trachea and the larynx, are capable of acting as eitherorigin 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 laryngealmuscles were simultaneously relaxed, contraction of the TL would produce a re-traction 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 cranialparts of the tracheolateralis (TL) and tracheohyoideus (TH) muscles, together with simul-taneous relaxation of the rostral extrinsic laryngeal muscles (REL) and passive stretch of thearytenoglossal ligaments (AGL), produces a retraction of the larynx (L) and telescoping of therostral segments of the trachea. Simultaneously the activated stemotrachealis (ST) under-goes active stretch by the TL, 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 ETMS and S T muscle cannot exceed that produced in theREL and AGL. ICS: boundary of the interclavicular air sac. The TH is shown displaced fromthe mid-line where it normally runs alongside the trachea.

caudal part of the TL, by exerting a caudorostral force on the tympanum, tends toremove the syrinx from the vocal configuration. This is borne out by the measureddecrease in syringeal resistance shown in Fig. 1 and the abolition of pre-existing soundshown 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 vocaliza-tion 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 theaxial 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 muscularactivity may explain the production of certain types of high-pitched wailing soundswhich occur in chickens. Simultaneous recordings of tracheal pressure and muscleactivity suggest that airflow is relatively unimpeded and that the ETMs are being heldtaut by strong contraction of the TL. Gaunt and Gaunt propose that contraction ofthe TL, by stabilizing its joint insertion with the ST also permits the latter to exertsufficient tension on the syringeal ligament to draw the pessulus forward and relax theposterior margin of the membranes. Only a very slight movement of the pessulusappears 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 alsoactive during normal breathing. They proposed that its chief function was to maintainthe patency of the airway against adverse positive pressures in the ICS although ofcourse this was also compatible with a steering role for the syrinx during vocalization.Gaunt & Gaunt (1977) expressed reservations on the normal respiratory functionof 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 in-spiratory activity in the TL during stressed breathing in anaesthetized birds. Sinceresting respiratory pressures never exceed + 1-2 cm H2O (1-2 x ioe N m~2) therewould seem little danger of ETM collapse in normal conditions. Moreover, owing tothe 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 thateven large hydrostatic pressures in the ICS will be equalized across the ETMs, so longas 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 duringeither expiration or inspiration.

White (1968) recognized the importance of the TL and TH (her 'caudal extrinsiclaryngeal muscles') in bringing about a gross retraction of the larynx during crowingin cockerels. Powerful retraction of the larynx in response to direct stimulation ofthese 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 ispossible that the resultant decrease in overall tracheal length and tracheal resistancemight influence the efficiency of the syringeal mechanism. Fig. 5 demonstrates thesensitivity of the mechanism to alterations in downstream pressure and resistance;any means that led to a reduction in the potentially large tracheal pressures resultingfrom the dramatically increased airflows during vocalization (Brackenbury, 1977)would be advantageous to sound production.

White (1968) and Gaunt & Gaunt (1977) have suggested another possible functionfor laryngeal retraction: to influence sound quality by altering the shape of the pharyn-geal cavity. Audiospectrograms of crowing in adult chickens show it to be very rich inovertones (Collias & Joos, 1953; Konishi, 1963; Wood-Gush, 1971) but these seemto be governed by tracheal length and ETM tension (Harris, Gross & Robeson, 1968;Abs, 1969; Gaunt & Wells, 1973; Lockner & Murrish, 1975). The characteristictonal 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 fullactivity 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 muscleswill not silence birds (Miskimen, 1951; Youngren et al. 1974; Smith, 1977; Bracken-bury, 19786) and Gross (19746) was led to the conclusion that it is almost impossibleto abolish sound production by any means short of serious interference with therespiratory 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 theETMs; the extra effort in operated animals suffices to bring the relaxed membranesto 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 theaudiogenerator at relatively low air-sac pressures and airflow rates; indeed they maybe indispensable for the production of low volume sounds that require minimalphysical effort. In contrast, during crowing the normal muscular controls in favourof economy of effort appear to be sacrificed in order to obtain maximum sound outputat maximum possible airflow rates. From their comparison of audio-spectrograms ofnormal crowing and of sounds elicited from excised syrinxes Harris et al. (1968) dedu-ced that the ETMs must be held in a position of near maximal stretch throughoutthe crowing cycle. This would imply that the TL undergoes powerful contractiononly weakly opposed by the much smaller ST muscle. The latter may serve partly as aligamentar 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 canexert maximal retractile force on the larynx. Moreover, the same anchorage may alsoallow the ST to stretch the syringeal ligament and relax the ETMs as described byGaunt and Gaunt in their analysis of the wail in chickens.

At the same time insurance against excessive tensile pull on the syrinx and STmuscles is procured by a novel means. For, as White (1968) reasoned, retraction ofthe larynx must be accompanied by relaxation of the rostral extrinsic laryngeal musclesand stretch of the aryteno-glossal ligaments, both of which connect the larynx to thehyoid. This means that the tension generated by the TL is relayed to elastic elementsat the rostral end as well as at the caudal end (Fig. 6). Physical considerations dictatethat the tension in the ST and syringeal membranes cannot exceed that in the rostralelastic elements. Both sets of elements also serve to limit the contractile force generatedby 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 sluggishcontractile 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 unimpededairflow. The advantages may be twofold: first, since the total fluid power availablefor driving the membranes is proportional to airflow2 (Brackenbury, 1979a) it paysdouble dividends to minimise flow obstruction; second, it is possible that very highflow 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 amplitudesand consequent overloading of the membranes (Brackenbury, 19796).

Airflow resistance during vocalization

The observed increase in airway resistance during crowing has previously beenascribed mainly to the partial occlusion of the syringeal lumen by the ETMs but alsopartly to purely aerodynamic forces that cause the pressure/flow relationship to risenon-linearly at higher flow rates (Brackenbury, 19786). Amongst these forces, thosedue to turbulent airflow through the syrinx seem the strongest candidate. If, as aresult of the contraction of the TL muscle, the syringeal lumen is not occluded to theextent previously envisaged, a greater attribution must be made to this turbulentsource of resistance.

Neural control of muscles of the anterior respiratory tract

The ST, TL and TH are hypobranchial muscles derived from ventral extensions ofthe post-occipital somites of the embryo and thus share a common innervation by thehypoglossal nerve, with the intrinsic muscles of the hyoid and tongue and the rostralextrinsic muscles of the larynx (Weichert, 1970). Their primitive functional associa-tions are therefore with acts involving adjustment to the shape of the anterior res-piratory tract, such as deglutition, coughing and, in appropriate circumstances, res-piration. The association between respiratory movements and tracheal muscle activityis probably very loose during normal respiration but it becomes more evident duringdyspnea and thermal polypnea. The fluttering movements of the throat (gular flutter)of many birds during panting (Calder & Schmidt-Nielsen, 1968) involve the co-ordinated activity of the hyoid and extrinsic laryngeal muscles, including the TL andTH. It can be demonstrated that the cranial motor nuclei of the hypoglossal, as wellas the vagus and glossopharyngeal nerves, receive dual control by the panting centreand the respiratory centre (Brackenbury, 1978c). The hypoglossal nuclei, and themuscles that they serve, are thus amenable to control by at least two other centralareas 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 theextrinsic syringeal muscles be regarded as ' vocal' muscles. Truly vocal muscles existin the syrinx of passerine birds but virtually nothing is known about their detailedinnervation and control.

Voluntary inhibition of sound production

Natural physiological situations occur that involve the production of aerodynamicforces in excess of the threshold for passive sound production but for purposesentirely unrelated to vocalization, such as defaecation, preening and coughing. Fromthe experimental situation illustrated in Fig. 5 it can be inferred that an effectivedevice for reducing spurious sound production is active constriction of the glottis, forthis elevates tracheal resistance and impairs the syringeal mechanism and this isprecisely what appears to occur during defaecation and vigorous preening (Brackenbury19786).

This work was supported by the Science Research Council.

Sound production in the syrinx of the fowl 251

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