Download The functional anatomy of the rodent larynx in relation to audible

Zool. J. Linn Soc.. 56: 255-264. With 6 plates
April 1975
The functional anatomy of the rodent larynx
in relation to audible and ultrasonic crv
production
LAURENCE H.ROBERTS
Department of Zoology, King’s College, University of London *
Accepted for publication August I974
Rodents are well known for the production of physically quite different audible and ultrasonic
cries. Both of t h m cries are known to be produced in the larynx, but the anatomy of the
larynx is practically unknown, it thus being difficult to analyse how the cries are produced. The
anatomy of the larynx of Mus musculus is described in detail and is found to be essentially
typical of that of other mammals that can fix the thorax and make independent use of the
forelimbs. Unlike the larynx of microchiropteran bats, no modifications for ultrasound
production are apparent, although .the laryngeal structure is ideal for the production of audible
cries. However, the audible and ultrasonic cries differ so markedly that they are unlikely to be
produced by the same mechanism. The lack of laryngeal specialization therefore makes the
ultrasound production mechanism largely an enigma.
CONTENTS
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Introduction
Materials and methods
Resulai
Discussion
Acknowledgements
References
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INTRODUCTION
There is very little information available in the literature on the anatomy of
the rodent vocal tract and of the larynx in particular. The rodent larynx is
mentioned only briefly in the definitive work of Negus (1949) on the
comparative anatomy and physiology of the larynx, is not described, apart
from its blood supply and nerve supply, in Greene’s (1955) volume on the
anatomy of the rat and is not described by Keleman (1963). However, rodents
are now known for their wide range of vocalizations in a variety of behavioural
situations.
Not only do myomorph rodents produce their well-known audible cries, but
R m n t address: Department of Life Sciences, Polytechnic of Central London. 115 New Cawndish
Street, London W1M 8JS
18
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L. H. ROBERTS
both adults and young also produce ultrasonic cries in many behavioural
situations (Anderson, 1954; Zippelius & Schleidt, 1956; Noirot, 1965, 1966,
1968; Noirot & Pye, 1969; Sewell, 1967, 1968, 1969). Sewell (1970a) has
demonstrated the communication function of ultrasonic cries between the
mother and the young of Apodemus sylvaticus. and has investigated their role
in mating and aggression in the adults of various species (Sales, nCe Sewell,
1972a,b). Okon (1970a,b, 1971a,b, 1972) and Smith (1972) have shown that
tactile stimuli and cold stress motivate ultrasound production by young
rodents, probably to reduce maternal aggression and cause retrieval by the
mother respectively. Brown (1970, 1971a,b, 1973a,b) has shown a high degree
of auditory sensitivity at the levels of the cochlea and inferior colliculus in
several species, there being a second peak in the sensitivity curves at the
frequency of a species own ultrasonic cries as well as a peak in the audible
range.
Despite the greatly renewed interest in rodent vocal communication, there is
little information available on how the audible and ultrasonic cries are
produced. This, combined with the paucity of anatomical information on the
rodent vocal tract, makes it difficult t o produce a working hypothesis.
The audible cries and the ultrasonic cries differ considerably in their physical
structures. The audible cries consist of a fundamental, normally between 2 and
6 kHz, and a harmonic series exhibiting a formant structure. As such they are
typical of other mammalian “voiced” sounds where vibrating “vocal cords”
produce the fundamental and harmonic series, the fundamental is controlled by
muscle action and vocal tract cavity resonances produce the formant structure.
The best known example is human vowel production (Farnsworth, 1940;
Dunn, 1950; Stevens & House, 1955; House & Stevens, 1958; Fant, 1960;
Gopinath & Sondhi, 1970; or for brief reviews see Olson, 1967 or Holmes,
1972).
The ultrasonic cries of rodents may be of high intensity and are often pure
tones varying in frequency from 20-100 kHz or more from species to species.
Rapid frequency and amplitude changes may occur during a cry and often
instantaneous frequency and amplitude jumps occur with no obvious harmonic
relations. Simultaneous harmonically unrelated components may occur and
some cries, especially of cricetids, are broadband “huff“-like pulses (for reviews
of these sound structures see Sewell, 1970b or Roberts, 1973a). Such sound
structures are very difficult to explain in terms of vibrating structures and
muscle action, as are the changes in fundamental frequency of an audible cry t o
that of an ultrasonic cry. Whereas vocal tract cavity resonances appear to
influence the formant structures of audible cries, they do not appear to
influence the ultrasonic cries (Roberts, 1975).
Both types of cry have, however, been shown to be produced in the larynx
by nerve sectioning experiments (Roberts, 1973a, 1975). Both are produced at the same point in the respiratory cycle, at the onset of expiration
(Roberts, 1972a). The rate of air flow was found to be low during the sounds,
especially during ultrasound production, and to increase at the cessation of
sound. It was suggested that if rodents possess a valvular larynx typical of other
mammals that can fix the thorax and make independent use of the forelimbs
(Negus, 1949) sound production might be related t o a steady release of built-up
pressure through the valve system followed by a more rapid release at the
THE RODENT LARYNX
257
termination of the sound. Slight adjustment of the valves might then determine
whether vocal cords vibrate (although as yet there is only indirect evidence for
this in the literature), or whether ultrasound is produced by an as yet
unspecified mechanism.
As microchiropteran bats produce high intensity ultrasonic cries for
echolocation a comparison of the rodent larynx with their better known larynx
may be valuable. The microchiropteran larynx is relatively massive, the
cartilages often being unusually ossified and the muscles, especially the
cricothyroid muscle, may be highly developed (Robin, 1881; Elias, 1907;
Fischer 8t Gerken, 1961; Fischer & Vomel, 1961; Wassif 8t Madkour, 1968).
Associated with the larynx there may be unusual cavities in the form, for
example, of cartilaginous ampoules off the trachea below the larynx (Robin,
1881; Elias, 1907; Mohres, 1953; Wassif & Madkour, 1968). However, these
ultrasonic cries are produced by modified vocal cords (Griffin, 1958) and have
been proposed by Pye (1967) to be typical of other mammalian “voiced”
sounds comprising an harmonic series filtered by vocal tract resonances. This is
despite the fact that some of the echolocation cries may at first sight be similar
to certain rodent cries in consisting of a single component, although this is in
fact the second harmonic (Novick, 1958; Pye, 1968; Pye & Roberts, 1970;
Roberts, 1972b). The major points of Pye’s hypotheses have recently been
examined and discussed in detail with only slight modifications (Roberts,
1972b, 1973b).
I t would therefore appear that the ultrasounds of rodents and bats may be
produced by different mechanisms. In addition Negus (1949) does not note
any specializations of the rodent larynx similar to those described by other
workers for bats, although his description is limited to a few features. He
describes the laryngeal ventricles as being relatively shallow in the “brown rat”,
the lateral epiglottic folds as being absent and the aryteno-epiglottic folds as
forming the margins of the glottis. Nothing can be inferred about sound
production from such a description. An investigation of the anatomy of the
larynx in relation to sound production was therefore undertaken.
MATERIALS AND METHODS
The animals used for the histological work undertaken were three- and
four-day old “En strain” albino mice, Mus musculus (from an outbred strain
used by Eliane Noirot). Young mice were used as they were of a more suitable
size for sectioning. Before being sacrificed the animals were all tested for
normal audible and ultrasonic cry production.
Heads and necks were fixed for 24 hours in formal-acetic acid and then
decalcified in Pirenny’s fluid for 24 hours. The material was dehydrated in
alcohol, cleared with benzene and embedded in a plasticised wax, “Paramat”.
During embedding any traces of air were removed from the vocal tracts with a
weak vacuum produced by a water tap suction pump. Sections were cut at
10 pm using a rotary microtome. All the sections were mounted on slides and a
standard staining technique was employed using haematoxylin and eosin. In
addition cartilage was stained with toluidene blue. Five complete sets of
sections of the heads and necks were prepared; two of saggital sections (hence
dorso-ventral longitudinal sections of the larynx), one of transverse sections of
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L. H. ROBERTS
the neck (hence transverse.sections of the larynx) and two of coronal sections
(hence approximately lateral longitudinal sections of the larynx).
Microscopic analysis of every section was undertaken, sections being
compared by scale drawings produced using a camera lucida. A micrometer
slide was used for calibration.
RESULTS
The laryngeal skeleton and associated soft tissues were found to be well
developed in all five animals. The laryngeal cartilages were quite typical with
none of the modifications shown by the microchiropteran larynx (Robin,
1881 ; Elias, 1907; Wassif & Madkour, 1968). No unusual cavities were found to
be associated with the larynx.
The cricoid cartilage was found to be a signet ring shape, being deep dorsally,
narrowing laterally and being fairly narrow ventrally lying just posterior to the
thyroid cartilage in this region (Plates lA, B, 2A, 4A, B and 6A). Dorsally the
cricoid extends back to overlie the first two tracheal rings whereas ventrally it
does not (Plates l B , 3B, 4 B and 6A). On the anterior dorsal surface are the
articulations with the paired arytenoid cartilages (see below) and ventrally a
fine connective tissue membrane links the cricoid and thyroid cartilages
forming the cricothyroid membrane (Plates l B , 3B and 4A). The anterior
margin of the cricoid extends further towards the glottis dorsally than
ventrally.
The thyroid cartilage is loosely associated with the hyoid bone and more
closely associated with the cricoid cartilage. The hyoid lies transversely under
the base of the tongue anterior to the ventral plate of the thyroid (Plates l A , B,
2B, 3B, 4A, 5A and 6A) and extends around the lateral regions of the pharynx.
Dorso-lateral extensions of the thyroid cartilage, the superior cornua, reach
forward to be associated by ligaments with the dorsal extensions of the hyoid
on each side (Plate 5A). The thyroid and cricoid cartilages articulate at the tip
of the inferior cornu of the former, the cricothyroid joint so formed on the
dorso-lateral surface of the cricoid appearing to be quite firm (Plates 2A,B).
The thyroid alae, making up the body of the thyroid cartilage, are complete
ventrally (Plates 2A and 3A,B and others) and, as is typical for other mammals,
incomplete in the dorsal region just reaching the dorso-lateral margins of the
cricoid cartilage. The thyroid alae are broad and typically horseshoe-shaped in
transverse section (Plate 3A).
The antero-superior region of the thyroid cartilage bears a condensation of
cartilage which extends into the epiglottis as the epiglottic cartilage (Plates 1B,
3B, 4A and 6A). This raises the anterior and antero-lateral margins of the
glottis (seen in saggital section in Plate 3B and in horizontal section in
Plate 2B). Lateral to the margins so formed are the lateral food channels
leading to the oesophagus. As Negus (1949) pointed out, the lateral margins of
the glottis are the arytenoepiglottic folds. A muscle runs from the epiglottic
cartilage into the tongue, contraction of which will lower the epiglottis. The
epiglottis lies in an intranarial position in the sections of some animals and
under the soft palate in others; it may therefore by mobile. In the lateral
regions of the joint of the thyroid and epiglottic cartilages may be seen small
THE RODENT LARYNX
259
condensations of cartilage extending into and supporting the margins of the
glottis. These are the cartilages of Wrisberg (Plates 4A and 6A).
Each of the pair of arytenoid cartilages is articulated on the dorso-lateral
anterior surface of the cricoid cartilage at the closely fitting cricoarytenoid
joints (Plates lA, 3A and 4B). Lateral to the joint is a short muscular process
(Plate 5A) and medial to the joint an extension from the main body of the
arytenoid, the vocal process, extends slightly diagonally to the margin of the
glottis (Plates 4A and SB). Dorsally the arytenoids bear the cartilages of
Santorini that support the posterior margin of the glottis and the entrance to
the oesophagus (Plates 1 B and 6A). Between the cartilages of Santorini and the
epiglottic cartilage and cartilages of Wrisberg run the upraised margins of the
glottis, lateral to which are the food channels.
The muscles associated with the larynx are, like the cartilages, little modified
from the typical mammalian form. However, as with the laryngeal skeleton, the
muscles are very well developed in the animals examined. The suspensory and
associated external muscles of the larynx are largely outside the scope of this
study but the major ones can be described quite simply. The inferior
pharyngeal constrictor muscles running from the dorso-lateral surface of the
thyroid and cricoid cartilages around the oesophagus can be seen in Plates 3A
and 5B. The main suspensory muscle of the larynx, the thyrohyoid, can be seen
in Plates lA, 2B, 3B, SA and 6B. The sternothyroid muscle can be seen in
Plates 2B and 6 B and the sternohyoid muscle in Plates 4A, SA and 6A.
Quite typically the muscles that move the parts of the larynx relative to each
other and hence might control vocalization can be divided into three groups,
the external adductors, the internal adductors and the internal abductors. The
external adductor group is comprised of one pair of muscles, the cricothyroids,
running from the anterior of the cricoid near the mid line to the thyroid ala
and inferior cornu of the thyroid (Plates 2A,B). The muscle appears to be quite
well developed in the specimens examined, but its action appears to be quite
normal in approximating the anterior parts of the thyroid and cricoid by
rotation around the cricothyroid joint and thus elongating the glottis and
adducting the arytenoids as a result. A major role for this muscle has been
proposed to be a bracing action for sound production. The bracing action
certainly appears to be a feasible function for this muscle in rodents.
The internal adductors, or sphincters, comprise the interarytenoid muscle,
the paired lateral cricoarytenoid muscles and the paired thyroarytenoid
muscles. The interarytenoid muscle is very small; movement of the arytenoids
towards one another may therefore be weak. The lateral cricoarytenoid muscles
(Plates lA, 4 B and SA) run from the lateral part of the cricoid to the muscular
process of the arytenoids. Their action is to draw the arytenoids towards the
glottis approximating the vocal processes. This action might be important,
together with the bracing action of the cricothyroids, in “voiced” sound
production. The remaining part of the sphincter ring, the paired thyroarytenoid
muscles, are important in vocalizing animals and the rodent larynx appears to
be no exception. The thyroarytenoids make up the superior and lateral part of
the adductor group (Plates l A , B, 2B, 3A, 4B, SA, B and 6A). The muscles are
large and run mainly from the arytenoids to the middle of the thyroid alae
(Plates lA, 3A and 4B). The specimens examined show a well developed but
relatively shallow ventricle on each side of the larynx dividing the fold of tissue
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L. H. ROBERTS
running from the arytenoids to the thyroid on each side into a superior and
inferior thyroarytenoid fold (Plates 38, 4A and 6A). The bulk of the
thyroarytenoid muscle underlies the inferior fold only (Plates lB, 2B and
6A,B). Whereas part of the muscle lies in close proximity to the inferior fold,
the superior fold appears to be lacking in muscle tissue (Plate 6A) although
some of the muscle may lie more deeply under this fold. This is somewhat
different from the arrangement of the muscle for example in man, where there
are distinct superior and inferior divisions associated with the superior and
inferior thyroarytenoid folds. However, as in man, the muscle can be divided
into internal and external portions (Plate SB). The internal part lies in close
proximity to the inferior thyroarytenoid fold and runs from the vocal process
of the arytenoid to the cricothyroid membrane and to an extension of that
membrane, the conus elasticus, that runs to the margins of the glottis
(Plate 6B). The close association of the internal division of the thyroarytenoid
muscle and the margin of the glottis may be seen in Plate 5B. The external
division of the muscle is its main bulk, running from the body of the arytenoid
to the thyroid ala. The action of the thyroarytenoid muscle is to shorten and
tense the inferior thyroarytenoid folds and oppose the vocal processes of the
arytenoids.
The internal abductor muscles are represented by the paired posterior
cricoarytenoid muscles running from the muscular processes of the arytenoids
to a wide area of the posterior surface of the cricoid (Plates l A , B, 2A, 3B, 4A,
B and 5A,B). The action of these muscles alone will open and lengthen the
glottis. The action of the sphincter group of muscles alone will shorten and
close the glottis and as with other mammals (Negus, 1949) this may be
important during deglutition. Again, as in other mammals when opposed by the
dilator muscles the sphincters may be especially important for sound
production.
In most mammals with laryngeal ventricles the inferior thyroarytenoid folds,
tensed by the thyroarytenoid muscles, act as the “vocal cords’’ for “voiced”
sound production (Negus, 1949). The rodent larynx would appear to be no
exception to this. Although the inferior folds are not very sharp in the
specimens examined the functional arrangement appears to be ideally suited for
a typical voice production mechanism. In the rodents the function of the
superior folds, considering the lack of intrinsic muscle tissue, is more difficult
to interpret. Where there is a well developed musculature, as in man, the
superior folds are thought to act as valves to prevent air leaving the lungs, thus
aiding fixation of the thorax. It is possible in the rodent larynx that more
remote musculature is capable of bringing about this action. The relatively
blunt inferior folds may function as inlet or outlet valves as required.
DISCUSSION
The rodent larynx, at least that of Mus musculus. clearly has none of the
modifications for ultrasound production possessed by the larynx of microchiropteran bats. There is none of the massive development of laryngeal
cartilages and associated musculature nor the unusual structure of the inferior
and superior thyroarytenoid folds or the development of cavities off the vocal
tract. However, the ultrasonic cries of bats are specialized voiced sounds
THE RODENT LARYNX
26 1
produced by the modified “vocal cords” (Griffin, 1958; Novick & Griffin,
1961; Pye, 1967, 1968; Roberts, 1972b, 1973b), whereas rodents produce
quite typical mammalian audible cries as well as their ultrasonic cries from the
larynx (Roberts, 1975).
The rodent larynx is clearly well developed at an early age, but care must be
taken in assuming that this development is solely for sound production as the
larynx is involved in the control of respiratory airflow and prevention of
inundation by food material as well as sound production. However, it is quite
clear from the description of laryngeal anatomy of mouse pups given here that
the larynx is ideally suited for the production of audible cries by a normal
mammalian voice mechanism (as discussed in the introduction). I t is also clear,
however, that the physical structures of the audible and ultrasonic cries differ
so markedly that it is most unlikely that they are produced by the same
mechanism for the reasons discussed in the introduction t o this paper. There
are, though, no apparent modifications to the rodent larynx for ultrasound
production. Therefore little information on the ultrasound production
mechanism can be gained from the study of the anatomy of the larynx, except
perhaps that the mechanism must be an unusual one.
Although there are strong indications of two distinct sound production
mechanisms in the rodent larynx, two factors suggest that the mechanisms are
closely related in some ways. Firstly, the respiratory patterns are very similar
during audible and ultrasonic cry production (Roberts, 1972a), indicating that
the valve systems of the larynx might be acting in similar ways in each case.
Secondly, the two cry types may on occasions be closely linked physically as
one can break almost instantaneously into the other, but they do not occur
simulataneously (Roberts, 1972a, 1973a). This might indicate that only a fine
adjustment of the valve system is needed t o switch from a typical voiced
mechanism t o an as yet unspecified ultrasound production mechanism or vice
versa.
Evidence from the structure of the rodent ultrasonic cries and experimental
evidence is now indicating that ultrasound production is based on a specialized
whistle mechanism (to be published elsewhere), and that this is in no way
incompatible with the results reported here and with the discussions above.
ACKNOWLEDGEMENTS
I would like to thank Mr John Wells of King’s College, University of London
for his advice on histological techniques, and Professor J. D. Pye for his advice
and encouragement throughout the work reported here. I would also like to
thank Professor D. R. Arthur for providing the facilities for carrying out the
histological preparation in King’s College, Department of Zoology and
Professor N. Singer, Head of the Department of Life Sciences of The
Polytechnic of Central London for providing facilities for detailed analysis of
the material and photographic facilities. The initial part of this work was
carried out during the tenure of a Science Research Council studentship.
262
L. H. ROBERTS
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ABBREVIATIONS USED IN PLATES
ant.
d
A
An
Ab
B
C
e
cb
D
E
F
c
H
I
J
anterior
dorsal
arytenoid cartilage
muscular process of arytenoid
cartilage
vocal process of arytenoid cartilage
cricoid cartilage
thyroid cartilage
inferior cotnu of thyroid cartilage
superior comu of thyroid cartilage
hyoid bone
cricoarytenoid joint
cricothyroid joint
tracheal cartilage
epiglottic cartilage
cartilage of Santorini
cartilage of Wrisberg
K
L
M
N
0
P
Q
R
S
T
U
V
W
X
Y
z
inferior constrictor muscle
thyrohyoid muscle
sternohyoid muscle
sternothyroid muscle
cricothyroid muscle
lateral cricoarytenoid muscle
thyroarytenoid muscle
posterior cricoarytenoid muscle
cricothyroid membrane
conus elasticus
ventricle
superior thyroarytenoid fold
inferior t hyroarytenoid fold
buccal cavity
palate
-phagus
EXPLANATION OF PLATES
PLATE 1
A. Saggital section of the larynx of an albino mouse pup lateral to the mid-line through the side
of the cricoid cartilage and lateral part of one arytenoid cartilage.
B. Saggital section of the Iarynxpf an albino m o m pup, closer to the mid-line than that of A,
through the bulk on one arytenoid cartilage.
PLATE 2
A. Transwrse section of the larynx of an albino mouse pup through the cricoid cartilage,
showing the joint of the cricoid with the inferior comu of the thyroid cartilage.
B. Longitudinal horizontal section of the larynx of an albiao m o m pup (the section is not M
exact horizontal plane, the right half Wig slightly more ventral).
264
L. H. ROBERTS
PLATE 3
A. Transverse section of the larynx of an albino mouse pup at the level of the thyroid cartilage
(above the level of the section shown in Plate 2A).
B. Soggital section of the larynx of an albino mouse pup slightly lateral to the mid-line
(posteriorly the section passes through the medial part of one arytenoid cartilage rather than
between the arytenoids).
PLATE 4
A. Saggital section of the larynx of an albino mouse pup taken a little laterally to that in
Rate 3 8 .
B. Saggital section of the larynx of an albino mouse pup lateral to the mid-line through the
lateral part of the cricoid ring, showing the thyroarytenoid muscle underlying the thyroarytenoid folds and the cricoarytenoid joint.
PLATE 5
A. Saggital section of the larynx of an albino mouse pup through the lateral part of the
arytenoid cartilage. the muscular process (i.e. more lateral to the section in Plate 4B).
B. Transverse section of the larynx of an albino mouse pup at the level of the vocal processes of
the arytenoid cartilages.
PLATE 6
A. Saggital section of the larynx of an albino mouse pup through the bulk of one arytenoid
cartilage and the innermost margin of the cricoid ring (i.e. slightly lateral to the section shown
in Plate 4A).
B. Longitudinal horizontal section o f the larynx of an albino mouse pup through the bulk of
the thyroid cartilage (i.e. at a lower level than the section shown in Plate 28).
2001.
J . Linn. SOC.,
56 (197s)
L. H. ROBERTS
Plate 1
(Facingp. 264)
2001.J. Linn. SOC.,
56 (197.5)
L.
H.ROBERTS
Plate 2
2001.7. Linn. Soc.. 56 (1975)
L. H. ROBERTS
Plntc 3
2001.J . Linn. SOC..56 (1975)
Plate 4
Zod. J. Linn. SOC.,
56 (1975)
L. I I . ROBERTS
Plate 6
%d.J. Litin. Soc., 56 ( 1975)
I
1,. 14. ROBERTS
Imm
I.