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Mechanics of the exceptional anuran ear

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The anuran ear is frequently used for studying fundamental properties of vertebrate auditory systems. This is due to its unique anatomical features, most prominently the lack of a basilar membrane and the presence of two dedicated acoustic end organs, the basilar papilla and the amphibian papilla. Our current anatomical and functional knowledge implies that three distinct regions can be identified within these two organs. The basilar papilla functions as a single auditory filter. The low-frequency portion of the amphibian papilla is an electrically tuned, tonotopically organized auditory end organ. The high-frequency portion of the amphibian papilla is mechanically tuned and tonotopically organized, and it emits spontaneous otoacoustic emissions. This high-frequency portion of the amphibian papilla shows a remarkable, functional resemblance to the mammalian cochlea.
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REVIEW
Mechanics of the exceptional anuran ear
Richard L. M. Schoffelen Æ Johannes M. Segenhout Æ
Pim van Dijk
Received: 9 July 2007 / Revised: 11 March 2008 / Accepted: 14 March 2008 / Published online: 3 April 2008
The Author(s) 2008
Abstract The anuran ear is frequently used for studying
fundamental properties of vertebrate auditory systems. This
is due to its unique anatomical features, most prominently
the lack of a basilar membrane and the presence of two
dedicated acoustic end organs, the basilar papilla and the
amphibian papilla. Our current anatomical and functional
knowledge implies that three distinct regions can be iden-
tified within these two organs. The basilar papilla functions
as a single auditory filter. The low-frequency portion of the
amphibian papilla is an electrically tuned, tonotopically
organized auditory end organ. The high-frequency portion
of the amphibian papilla is mechanically tuned and tono-
topically organized, and it emits spontaneous otoacoustic
emissions. This high-frequency portion of the amphibian
papilla shows a remarkable, functional resemblance to the
mammalian cochlea.
Keywords Amphibian Anuran Frog
Auditory system Inner ear mechanics
Introduction
The anatomy and physiology of the amphibian ear show
both remarkable resemblances and striking differences
when compared to the mammalian auditory system. The
differences between the human and the amphibian auditory
system are too significant to warrant direct generalizations
of results from the animal model to the human situation.
However, studying hearing across species helps to under-
stand the relation between the structure and function of the
auditory organs (Fay and Popper 1999). Thus, we hope and
expect that the knowledge gained about the amphibian
auditory system fits into our understanding of auditory
systems in general.
Over the course of history, a number of diverse
amphibian species developed. Currently only three orders
remain: anurans, urodeles, and caecilians. Their evolu-
tionary relationship, as well as the evolutionary path of the
individual orders, is still under debate. However, they are
generally grouped into a single subclass, Lissamphibia of
the class Amphibia (Wever 1985).
The ancestral lineage of amphibians separated from the
mammalian lineage, approximately 350 million years ago,
in the paleozoic era. Many of the important developments
in the auditory systems emerged after the ancestral paths
separated (Manley and Clack 2003). This implies that
shared features, like the tympanic middle ear, developed
independently in different vertebrate lineages.
The anurans -frogs and toads- form the most diverse
order of amphibians. The living species are classified into
two suborders, Archaeobatrachia and Neobatrachia
(Wever 1985). Both within and between these suborders,
there is a large variation in the anatomy and physiology of
auditory systems. The most thoroughly studied species
belong to the family Ranidae, as is reflected in the work
referenced in this paper.
The hearing organs of anurans are often falsely assumed
to be more primitive than those of mammals, crocodiles,
and birds. The relatively simple structure and functioning
R. L. M. Schoffelen J. M. Segenhout P. van Dijk
Department of Otorhinolaryngology/Head and Neck Surgery,
University Medical Center Groningen, P.O. Box 30001,
9700 RB Groningen, The Netherlands
R. L. M. Schoffelen (&) P. van Dijk
School of Behavioral and Cognitive Neuroscience,
University of Groningen, P.O. Box 196,
9700 AD Groningen, The Netherlands
e-mail: r.l.m.schoffelen@rug.nl
123
J Comp Physiol A (2008) 194:417–428
DOI 10.1007/s00359-008-0327-1
of the amphibian ear offer an excellent possibility to study
hearing mechanisms (e.g., Ronken 1990; Meenderink
2005). On the other hand, the sensitivity of the frog inner
ear, which appears to be able to detect (sub)angstrøm
oscillations (Lewis et al. 1985), shows that the frog ear
functions as a sophisticated sensor.
While the ears of most vertebrate species contain one
dedicated acoustic end organ, the frog ear has two, the
amphibian papilla and the basilar papilla.
1
Like in other
vertebrates, these organs contain hair cells for the trans-
duction of mechanical waves into electrical (neural)
signals. In mammals, birds and lizards, the hair cells are set
on a basilar membrane. The frog inner ear lacks such a
flexible substrate for its sensory cells. The hair bundles of
the frog’s auditory organs are covered by a tectorial
membrane, as they are in all terrestrial vertebrates except
for some lizards species (Manley 2006).
In mammals, the mechanical tuning of the basilar
membrane is the primary basis for frequency selectivity. In
the absence of the basilar membrane, the frog’s auditory
organs must rely solely on the tectorial membrane and on
the hair cells themselves for frequency selectivity.
Recently, Simmons et al. (2007) and Lewis and Narins
(1999) published reviews of the frog’s ear anatomy and
physiology. In the current paper, we focus on the
mechanics of the inner ear, specifically on the mechanics of
the tectorial membrane. Only one publication exists on
direct mechanical/acoustical measurements of structures in
the frog inner ear (Purgue and Narins 2000a). Therefore,
many of our inferences will result from indirect manifes-
tation of inner ear mechanics, as observed in anatomical,
electro-physiological and otoacoustic-emission studies.
Nevertheless, these studies provide a consistent view of the
mechanics of the anuran inner ear.
Anatomy
Middle ear
The ears of most terrestrial vertebrates can be divided into
three principal parts: the outer ear, the middle ear and the
inner ear. In mammals, the outer ear consists of a pinna and
an ear canal, which terminates at the tympanic membrane.
In most frog species the outer ear is absent,
2
and the
tympanic membrane is found in a bony ring, the tympanic
annulus, in the side of the skull.
The tympanic membrane defines the distal boundary of
the middle ear cavity. This air-filled cavity is spanned by
the ossicular chain, which serves to transfer vibrations of
the tympanic membrane to the oval window of the inner
ear. In the frog, the ossicular chain consists of two struc-
tures, the extra-columella and the columella (Jørgensen and
Kanneworff 1998; Mason and Narins 2002a). The carti-
laginous extra-columella is loosely connected to the center
of the tympanic membrane. Medially, it flexibly connects
to the partially ossified columella. The columella widens to
form a footplate at its medial end, where it attaches to the
oval window of the inner ear. Acoustic stimuli primarily
enter the inner ear through the oval window.
The middle-ear’s primary function is to compensate for
the impedance mismatch between the air and the fluid-
filled inner ear. There are two contributions to this com-
pensation (Jaslow et al. 1988; Werner 2003). The first
contribution results from the small area of the oval window
relative to the area of the tympanic membrane. This causes
a concentration of the external force exerted on the tym-
panic membrane. The second contribution involves a lever
action of the columella footplate. The footplate attaches to
the otic capsule along its ventral edge. This bond is sug-
gested to be the location of the hinging point of the middle
ear lever in the frog (Jørgensen and Kanneworff 1998;
Mason and Narins 2002b). The lever action serves as a
force amplification mechanism and contributes to the
impedance matching between the outside air and the fluids
in the inner ear. Both effects result in pressure amplifica-
tion between the tympanic membrane and the columella
footplate, thus overcoming the impedance mismatch
between air and the inner-ear fluids.
An additional bony disk, the operculum, is flexibly
attached to the oval window in amphibians. The presence
of an operculum in anurans is unique among vertebrates.
The operculum’s position in the oval window can be
modulated through the m. opercularis, which also connects
it to the shoulder girdle.
The function of the operculum is not entirely clear.
Possibly, it serves to transfer substrate vibrations to the
inner ear (Lewis and Narins 1999; Mason and Narins
2002b). The putative path for these vibrations includes the
front limbs, the shoulder girdle and the m. opercularis
(Hetherington 1988; Wever 1985).
Alternatively, the operculum-columella system is pro-
posed to protect the inner ear’s sensory organs from
excessive stimuli. This protection hypothesis takes two
different forms. Wever (1985) suggests that the operculum
and the columella footplate can be locked together through
muscle action. In this manner, the flexibility of the con-
nection to the oval window decreases and the input
impedance increases, which in turn decreases the input
signal amplitude of the pressure wave in the inner ear. It
1
See the section Anatomy for an explanation of the anatomical
terms used.
2
Some species, like Amolops tormotus (Feng et al. 2006), have a
cavity in front of the tympanic membrane which is considered to be
an ear canal and thus an outer ear.
418 J Comp Physiol A (2008) 194:417–428
123
has also been suggested that the action of the m. opercu-
laris could uncouple the operculum and the footplate
(Mason and Narins 2002b). This would allow the opercu-
lum to move out of phase with the footplate. The out-of-
phase motion could absorb part of the inner ear fluid dis-
placement caused by the motion of the footplate.
Effectively this creates an energetic by-pass and decreases
the amplitude in the inner ear.
A tympanic middle ear, as described above, is con-
sidered to be the typical situation (Jaslow et al. 1988),
which can be found in the family Ranidae. However, a
wide range of variations in middle ear structures is found
across species. In some species, a bony disk occupies the
tympanic annulus rather than a membrane, for example,
Xenopus leavis (Wever 1985), and there are a number of
‘earless’ frogs. The tympanic membrane and the tym-
panic annulus are absent in these species. A functioning
inner ear and a partial middle ear usually exist, although
the middle ear cavity may be filled with connective tissue
(e.g., Telmatobius exsul, Jaslow et al. 1988), or not exist
at all (e.g., species in the Bombina family, Hetherington
and Lindquist 1999; Wever 1985). Remarkably, some of
these ‘earless’ frogs have a mating call and exhibit
neurophysiological responses (Bombina bombina, Walk-
owiak 1988; Atelopus, Lindquist et al. 1998) at typically
auditory frequencies, which implies they have another
path for the transfer of airborne sound to the inner ear
(Jaslow et al. 1988), for example, through the lungs
(Narins et al. 1988; Lindquist et al. 1998; Hetherington
and Lindquist 1999).
Inner ear
The inner ear in the frog has two membranous windows:
the oval window and the round window. As mentioned
above, acoustic energy primarily enters the inner ear
through the oval window. The round window is the main
release point of this energy (Purgue and Narins 2000a). A
similar lay-out can be found in other terrestrial vertebrates.
However, the round window of the frog does not open into
the middle ear as it does in mammals. Rather, it can be
found in the top of the mouth cavity, under a lining of
muscle tissue.
Within the inner ear, there are two intertwined mem-
branous compartments: the perilymphatic and the
endolymphatic labyrinths (see Fig. 1). The perilymphatic
labyrinth connects to both the oval window and the round
window. Starting at the oval window and going medially, it
passes through a narrow foramen, and widens into the otic
cavity, forming the periotic cistern. Continuing medially it
narrows again into the periotic canal. This canal connects
the periotic cistern with the perilymphatic space at the
round window (Purgue and Narins 2000b).
Between the lateral perilymphatic cistern and the round
window, part of the endolymphatic space can be found.
The endolymphatic space also includes the semi-circular
canals located dorsally from the otic system. It contains the
sensory organs of hearing and balance. In the frog inner
ear, there are eight sensory epithelia (Lewis and Narins
1999; Lewis et al. 1985), located as follows:
three cristae in the semi-circular canals, which are
sensitive to rotational acceleration of the head,
and one each in:
the utricule, which detects linear acceleration,
the lagena, which detects both linear acceleration and
non-acoustic vibrations (Caston et al.
1977),
the sacculus, which is sensitive substrate vibrations up
to approximately 100 Hz, and also detects high level
low-frequency airborne sound, (Narins 1990; Yu et al.
1991)
the amphibian papilla, which detects low-frequency
acoustic stimuli (Feng et al. 1975), and
the basilar papilla, which is sensitive to high-frequency
airborne stimuli (Feng et al. 1975).
Hair cells are the sensory cells in all of these organs. Like
all hair cells, these cells have a stereovillar bundle on their
apical surface. Deflection of the bundle as a result of an
acoustical vibration or a mechanical acceleration, initiates
an ionic transduction current into the cell. This initial
current causes a cascade of ionic currents, eventually
resulting in the release of neurotransmitter at the basal
surface of the cell. The released neurotransmitter triggers
neural activity in the nerve fiber dendrites that innervate to
the basal portion of the hair cell (Pickles 1988; Yost 2000;
Keen and Hudspeth 2006).
As in most vertebrates, a tectorial membrane covers the
sensory cells of the auditory end organ. This membrane is a
polyelectrolyte gel, which lies on the stereovilli (Freeman
et al. 2003). The function of the tectorial membrane is not
well understood, and may vary between classes. However,
since the stereovilli in most vertebrate ears connect to this
membrane, it obviously plays an important role in the
conduction of acoustic vibrations to the hair cells.
3
Basilar papilla
The basilar papilla is found in a recess that opens into the
saccular space at one end, and is limited by a thin contact
membrane at the other. The contact membrane separates
3
In the mamallian ear, the inner hair cells, which are the primary
sensory cells, do not connect directly to the tectorial membrane.
However, their deflection is presumably closely associated with the
kinematics of the tectorial membrane (e.g., Nowotny and Gummer
2006).
J Comp Physiol A (2008) 194:417–428 419
123
the endolymphatic fluid in the papillar recess from the
perilymphatic fluid at the round window (Lewis and Narins
1999; Wever 1985). The recess perimeter is roughly oval in
shape; in the bullfrog, Rana catesbeiana, its major axis is
approximately 200 lm long, while the minor axis measures
approximately 150 lm (Van Bergeijk 1957). In the leopard
frog, Rana pipiens pipiens, it is of similar size (personal
observation, RLMS & JMS).
The oval perimeter of the lumen is formed from limbic
tissue; a substance unique to the inner ear, and similar to
cartilage (Wever 1985). The sensory epithelium is
approximately 100 lm long. It occupies a curved area that
is symmetrical in the major axis of the elliptical lumen. It
contains approximately 60 hair cells (measured in Rana
catesbeiana), from which the stereovilli protrude into the
lumen and connect to the tectorial membrane (Frishkopf
and Flock 1974). Typically the orientation of the hair cells,
as defined by the direction to which the v-shape of the
stereovilli bundle points (Lewis et al. 1985), is away from
the sacculus in Ranidae.
The tectorial membrane spans the lumen of the papillar
recess. It occludes about half the lumen, and consequently
takes an approximately semi-circular shape when viewed
from the saccular side (Frishkopf and Flock 1974; Wever
1985). The membrane has pores at the surface closest to the
epithelium, into which the tips of the hair bundles project
(Lewis and Narins 1999).
4
Amphibian papilla
The amphibian papilla can be found in a recess, that
extends medially from the saccular space and, in frogs with
derived ears, bends caudally to end at a contact membrane.
Like the basilar papilla’s contact membrane, the membrane
separates the endolymphatic fluid in the papilla recess from
the perilymphatic fluid at the round window.
The sensory epithelium is set on the dorsal surface of
this recess (Lewis and Narins 1999). The epithelium itself
has a complex shape; it consists of a triangular patch at the
rostral end, and an s-shaped caudal extension towards the
contact membrane (see Fig. 2). The exact shape and length
of the caudal extension varies across species, with the most
elaborate extensions occurring in species of the family
Ranidae (Lewis 1984), while some species lack the
s-shaped extension altogether (Lewis 1981).
In the epithelium, the hair cell orientation follows a
complicated pattern (see Fig. 2b). In the rostral patch the
cells are orientated towards the sacculus. On the rostral half
of the s-shaped extension, they are oriented along the
s-shape. However, on the caudal half, the orientation rotates
90 to become perpendicular to the s-shape (Lewis 1981).
An elaborate tectorial membrane is found on the hair
bundles. A bulky structure covers the rostral patch, while
the membrane gets thinner along the caudal extension
(Lewis et al. 1982). A tectorial curtain spans the papilla
recess approximately halfway between the sacculus and the
contact membrane (Shofner and Feng 1983; Wever 1985).
The curtain, also called the sensing membrane (Yano et al.
1990), spans the entire cross-section of the lumen. A small
slit in the tectorial curtain may function as a shunt for static
fluid pressure differences (Lewis et al. 1982).
Fig. 1 Schematic drawing of a
transverse section through the
frog ear (adapted from Wever
1985). The division into the
middle, and inner ear is
indicated above the image; a
selection of features is indicated
in the image. The colored
arrows indicate the paths of
vibrational energy: green
arrows represent the columellar
path, red arrows the putative
opercular path, and blue arrows
indicate the path through the
inner ear after combination of
the columellar and opercular
paths. The grey areas represents
endolympatic fluid, dark yellow
perilymphatic fluid. The green
areas indicate the tectorial
membranes in the papillae.
(Color figure is available in the
online version)
4
Some images from the basilar papilla suggest that there are free-
standing hair bundles in the anuran’s basilar papilla (e.g., Lewis et al.
1985). No conclusive proof or claim of this has been reported yet.
420 J Comp Physiol A (2008) 194:417–428
123
Response of the auditory end organs
As mentioned in the section Anatomy’, the oval window
serves as the primary entry point of acoustic energy into the
inner ear; the round window presumably serves as the
primary release point. After the energy passes through
the oval window, it enters the periotic cistern. Between this
relatively large perilymphatic space and the round window
there are two possible routes: through the endolymphatic
space, or through the periotic canal, bypassing the endo-
lymphatic space and the sensory organs altogether (Purgue
and Narins 2000a). The bypass presumably serves to pro-
tect the sensory organs against low-frequency over
stimulation (Purgue and Narins 2000b).
The vibrational energy that ultimately stimulates the
auditory end organs predominantly may enter the endo-
lymphatic space through a patch of thin membrane in its
cranial wall near the sacculus. This entry-point was iden-
tified by Purgue and Narins (2000b), by mechanically
probing the perimeter of the endolyphatic space. After
entering the endolymphatic space, the energy may pass
either through the basilar papilla’s or through the
amphibian papilla’s lumen to the round window.
Measurements of the motion of the respective contact
membranes show that there is a frequency-dependent sep-
aration of the vibrational energy between paths through the
amphibian and the basilar papilla (Purgue and Narins
2000a; see Fig. 3c). The accompagnying dynamic model of
the energy flow through the bullfrog’s inner ear (Purgue
and Narins 2000b) indicates that this separation may occur
based on the acoustic impedances of the paths.
The perilymphatic path through the periotic canal may
serve as a shunt for acoustical energy to the round window.
As its impedance exponentially increases with frequency,
low-frequency vibrations will most effectively utilize this
path. The endolymphatic path, on the other hand, pre-
sumably has a relatively constant impedance throughout
the frog’s auditory range. The respective lumina of the
amphibian and basilar papilla have a frequency-dependent
impedance of their own. According to the model mentioned
above, these impedances are dominated by the character-
istics of the contact membranes (Purgue and Narins)
(2000b). The respective peak displacements of the contact
membranes correspond to the detected frequencies in the
associated organs (Purgue and Narins 2000a).
Basilar papilla
The basilar papilla’s tectorial membrane is presumably
driven by a vibrating pressure gradient between the the
sacculus and the basilar papilla’s contact membrane. No
reports have been published on direct measurements of the
mechanical response of the tectorial membrane, or on the
basilar papilla’s hair bundle mechanics. However, the hair
cell orientation in the basilar papilla implies that the tec-
torial membrane’s primary mode of motion is to and from
the sacculus.
Auditory nerve fiber recordings from the frog basilar
papilla show a frequency selective response (see Fig. 4 for
examples of tuning curves). The range of characteristic
frequencies in nerve fibers from the basilar papilla is spe-
cies dependent. In the leopard frog, they are approximately
between 1,200 and 2,000 Hz (Ronken 1990); in the bull-
frog they are slightly lower, between 1,000 and 1,500 Hz
(Shofner and Feng 1981; Ronken 1991). In the Hyla-fam-
ily, the characteristic frequencies appear to be significantly
higher; in Hyla cinerea, the green treefrog, they range from
2.8 to 3.9 kHz (Ehret and Capranica 1980; Capranica and
Moffat 1983), and in Hyla regilla roughly from 2 to 3 kHz
(Stiebler and Narins 1990; Ronken 1991). Where studied in
other species, the characteristic frequencies of the basilar
papilla’s nerve fibers fall roughly within the bounds defined
by the bullfrog at the low end and the green treefrog at the
high end (Scaphiopus couchi: approximately 1-1.5 kHz,
Capranica and Moffat 1975; Ronken 1991
; Eleuthero-
dactylus coqui: approximately 2-4 kHz, Narins and
Capranica 1980, 1976; Ronken 1991; Physalaemus pustu-
losus group: around 2.2 kHz, Wilczynski et al. 2001).
In each individual frog, the tuning curves of the auditory
nerve fibers appear to have a nearly identical shape and
characteristic frequency (Ronken 1990; Van Dijk and
Meenderink 2006). This suggests that the entire basilar
papilla is tuned to the same frequency. Because of this
collective tuning, characterized by one characteristic
Fig. 2 Schematic drawing of the amphibian papilla of the bullfrog,
Rana catesbeiana, (adapted from Lewis et al. 1982), rotated to match
orientation of Fig. 1). TM Tectorial membrane, AP amphibian papilla.
a General overview of the AP; the dashed outline indicates the
location of the sensory epithelium, b hair cell orientation in the
sensory epithelium; dashed line indicates the position of the tectorial
curtain. The numbers along the perimeter indicate the characteristic
frequency of the auditory nerve fibers connecting to that site (in Hz)
J Comp Physiol A (2008) 194:417–428 421
123
frequency and a single tuning-curve shape throughout the
organ, the basilar papilla may be referred to as a ‘single
auditory filter’’. In comparison, the mammalian cochlea,
and the anuran amphibian papilla (see below), consist of a
combination of a large number of auditory filters (Pickles
1988).
The quality factor, Q
10dB
(e.g., Narins and Capranica
1976; Shofner and Feng 1981), is lower than that of other
vertebrate hearing organs in the same frequency range,
(Evans 1975; see Fig. 5), and ranges from approximately 1 to
2 in both the leopard frog and the bullfrog (Ronken 1991; see
Fig. 5). For other anuran species, the ranges are somewhat
a
g
f
e
d
c
b
h
Fig. 3 Overview of
measurements of the frog inner
ear; comparison between Rana
(left) and Hyla (right). The
dashed lines indicate the
separation between the
amphibian papilla and the
basilar papilla. a, b
Distributions of characteristic
frequencies of auditory nerve
fibers in Rana pipiens pipiens,
and Hyla cinerea. c Example of
the response of the contact
membrane in R. catesbeiana;
black line represents the
amphibian papilla, open
markers the basilar papilla.
d, e Distributions of
spontaneous otoacoustic
emissions in ranid species
(combined data from R. pipiens
pipiens and R. esculenta), and
hylid species (combined data
from H. cinerea, H.
chrysoscelis, and H. versicolor).
f Example of stimulus
frequency otoacoustic emissions
in R. pipiens pipiens at indicated
stimulus levels. g, h Examples
of DP-grams measured in Rana
pipiens pipiens, and Hyla
cinerea. a, b, d, e, g and h are
taken from Van Dijk and
Meenderink (2006). There they
were reproduced from Ronken
(1990), Capranica and Moffat
(1983), Van Dijk et al. (1989,
1996), Meenderink and Van
Dijk (2004), and Van Dijk and
Manley (2001), respectively. c
is taken from Purgue and Narins
(2000a), and f is an adapted
presentation of data from
Meenderink and Narins (2006)
(graph created with data
provided by Dr. Meenderink)
422 J Comp Physiol A (2008) 194:417–428
123
different, with the lowest minimum values (approximately
0.5) reported for Hyla regilla, and the highest maximum
values (approximately 2.8) in Scaphiopus couchi. Thus, the
basilar papilla’s frequency selectivity is relatively poor.
As illustrated in Fig. 3, there is no correspondence
between the range of characteristic frequencies in the
basilar papilla and the range of spontaneous otoacoustic
emission frequencies (Van Dijk and Manley 2001; Van
Dijk and Meenderink 2006; Van Dijk et al. 2003;
Meenderink and Van Dijk 2004, 2005, 2006; Meenderink
and Narins 2007). Since it is generally assumed that ot-
oacoustic emissions of a particular frequency are generated
at the detection site for this frequency, this suggests that the
basilar papilla does not generate spontaneous emissions.
However, it does emit distortion product otoacoustic
emissions (Van Dijk and Manley 2001), and stimulus fre-
quency otoacoustic emissions (Palmer and Wilson 1982;
Meenderink and Narins 2006). The peak amplitudes of the
distortion product otoacoustic emissions match the char-
acteristic frequencies of the auditory nerve fibers
innervating the basilar papilla (Meenderink et al. 2005).
The amplitude and phase characteristics of the distortion
product otoacoustic emissions can be qualitatively modeled
by assuming the basilar papilla to be a single passive non-
linear auditory filter (Meenderink et al. 2005). Thus, nerve
fiber recordings, otoacoustic emission measurements and a
model based on these measurements show that the basilar
papilla functions as a single frequency band auditory
receptor. This frequency band is relatively broad, and the
center frequency may depend on species and individual
animals.
The hypothesis that considers the basilar papilla as a
single resonator was originally put forward by (Van
Bergeijk 1957). He investigated the mechanical response of
the tectorial membrane in a scale model consisting of a thin
rubber tectorium spanning a lumen in a stiff wall. A
number of different vibration modes existed in this model.
Although Van Bergeijk’s model is vastly oversimplified,
the basic idea that the mechanical tuning of the tectorial
membrane may be the basis of the basilar papilla’s fre-
quency selectivity is still viable.
Amphibian papilla
As in the basilar papilla, the tectorial membrane in the
amphibian papilla is presumably driven by a vibrating
pressure difference between the sacculus and the round
window. Due to the more elaborate tectorial membrane
and the more complex pattern of hair cell orientations,
the motion of the membrane may be expected to be more
complex than that of the basilar papilla’s tectorial
membrane. The tectorial curtain is in the sound path
through the papilla, and presumably plays a role in
conveying vibrations to the tectorial membrane and the
hair bundles.
100
120
1000
4000
100
10dB
f
Frequency (Hz)
Threshold (dB SPL)
2.0
1.2
1.5
1.2
80
60
20
40
Fig. 4 Tuning curves measured in the auditory nerve in R. catesbei-
ana (unpublished measurements by JMS & PvD, 1992; various
specimens). The numbers in the graph indicate Q
10dB
values
Fig. 5 Comparison of the filter quality factor Q
10dB
versus the
characteristic frequency (CF, in kHz) of nerve fibers from the cat
cochlea (adapted from Evans 1975) and the leopard frog (adapted
from Ronken 1991). In the leopard frog graph, the triangular symbols
correspond to nerve fibers from the amphibian papilla; the circles to
fibers from the basilar papilla. The black line indicates the upper limit
of the amphibian papilla’s frequency domain. The grey area in the
upper (cat) graph corresponds to the area of the lower (frog) graph.
The loops indicate the approximate perimeter of the fiber populations
in the lower graph for the amphibian papilla and the basilar papilla.
J Comp Physiol A (2008) 194:417–428 423
123
Electrophysiological recordings from and subsequent
dye-filling of single fibers of the auditory nerve show that
the amphibian papilla has a tonotopic organization (Lewis
et al. 1982). The fibers innervating the triangular patch
have low characteristic frequencies, down to approximately
100 Hz. The frequencies increase gradually along the
caudal extension. In the bullfrog, the upper frequency is
about 1000 Hz; an overview of the tonotopic organization
is given in Fig. 2b.
5
The frequency selectivity of the amphibian papilla’s
nerve fibers is similar to that of mammalian auditory nerve
fibers with the same characteristic frequency. This is in
contrast to the significantly poorer frequency selectivity in
the basilar papilla’s nerve fibers (Ronken 1990; Evans
1975; see also Fig. 5).
In the low-frequency, rostral part of the papilla, the hair
cells are electrically tuned (Pitchford and Ashmore 1987;
Smotherman and Narins 1999). This tuning stems from the
electrical properties of the cell membrane’s ion channels.
The hair cell tuning characteristics parallels the tonotopy of
the single nerve recordings. Therefore, frequency selec-
tivity in the rostral part of the amphibian papilla appears to
be primarily determined by the electrical characteristics of
the hair cells.
However, there is a fundamental discrepancy between
the tuning characteristics of the hair cells and the auditory
nerve fibers. While hair cells exhibit a second-order reso-
nance (Pitchford and Ashmore 1987) auditory neurons
display a higher order filter characteristic (Lewis 1984).
Nevertheless, due to the parallels in the tonotopic organi-
zation, the assumption that the frequency selectivity is
determined by the electrical tuning seems viable for the
rostral part of the amphibian papilla. The higher-order
responses in the neural signal may result from coupling
between hair cells, which may be mechanical, for instance
through the tectorial membrane.
Neurons innervating the rostral portion of the amphibian
papilla display non-linear two-tone suppression similar to
that in other vertebrates (Capranica and Moffat 1980;
Benedix et al. 1994). Another manifestation of non-linear
behavior can be found in the response to noise: second-
order Wiener kernels of low-frequency neurons show
off-diagonal components, which are an indication of
non-linearity (Van Dijk et al. 1994, 1997). The spectro-
temporal receptive fields constructed from these Wiener
kernels exhibit suppressive side bands besides the main
characteristic frequency band of the fiber (Lewis and Van
Dijk 2004).
Hair cells caudal to the tectorial curtain do not display
electrical resonance (Smotherman and Narins 2000).
Therefore, the tuning of this high-frequency, caudal region
of the papilla must result from the mechanical properties of
the tectorial membrane and the hair cells.
Based on the hair cell orientation, displayed in Fig. 2b,
the tectorial membrane motion in the amphibian papilla is
expected to be far more complex than in the basilar papilla.
Assuming that the hair bundles are orientated in such a way
that they are maximally deflected by the connected tecto-
rial membrane, the rostral patch of the membrane should be
moving to and from the sacculus, if the appropriate stimuli
are presented. The rostral part of the s-shaped extension is
moving along its major axis, whereas the extension caudal
to the tectorial curtain should be moving in a transverse
direction.
The amphibian papilla appears to be the only source of
spontaneous otoacoustic emissions in the frog inner ear
(Van Dijk et al. 1989, 1996; Long et al. 1996; Van Dijk
and Manley 2001; Fig. 3d-e). The frequency distribution of
these emissions corresponds to the range of best frequen-
cies of the neurons projecting to the portion of the
amphibian papilla caudal to the tectorial curtain. It is
generally assumed that an otoacoustic emission of a spe-
cific frequency is generated at the location in the inner ear
where that frequency is detected. Under this assumption,
the presence of spontaneous otoacoustic emissions indi-
cates that the caudal portion of the amphibian papilla
exhibits spontaneous activity. Presumably, this activity is
related to active amplification of input signals in this area.
The caudal region of the amphibian papilla is also
involved in the generation of distortion product otoacoustic
emissions (Van Dijk and Manley 2001; Meenderink and
Van Dijk 2004
), and stimulus frequency otoacoustic
emissions (Meenderink and Narins 2006). The distortion
product otoacoustic emissions from the amphibian papilla
are more vulnerable to metabolic injuries than those from
the basilar papilla (Van Dijk et al. 2003). Also, both the
spontaneous (Van Dijk et al. 1996) and distortion product
(Meenderink and Van Dijk 2006) otoacoustic emissions
display a clear dependence on body temperature. These
results combine to indicate that the s-shaped extension of
the amphibian papilla caudal to the tectorial curtain func-
tions as an active hearing organ.
Discussion
Our aim in this review is to outline what is known about the
mechanical response properties of the amphibian and basi-
lar papilla. Only one published report exists of the direct
5
In some species of the Hyla-family the upper frequency in the
amphibian papilla is markedly higher than in the bullfrog (Ronken
1991), up to approximately 2.8 kHz in H. cinerea (Ehret and
Capranica 1980). However, even in these species the vast majority of
the recorded fibers from the amphibian papilla have best frequencies
below 1250 Hz.
424 J Comp Physiol A (2008) 194:417–428
123
mechanical measurements of structures associated with
these papillae (Purgue and Narins 2000a). The measure-
ments show that the response of the contact membrane is
frequency dependent for each papilla. The movement of
the contact membrane may be assumed to reflect the fluid
motion within the respective papilla. The contact mem-
brane of the amphibian papilla shows a maximum response
when the ear is stimulated with relatively low acoustic
frequencies, while the basilar papilla contact membrane
exhibits a maximum response to higher frequencies.
The amphibian and the basilar papilla are the only
hearing organs found in terrestrial vertebrates in which the
hair cells are not on a flexible basilar membrane. Instead
the hair cells are embedded in a relatively stiff cartilagi-
nous support structure. Any frequency selective response,
therefore, most likely originates from the mechanical or
electrical properties of the hair cells, or the mechanical
properties of the tectorial membrane, or a combination of
these factors. Since there are no direct mechanical mea-
surements of either the hair cells in the papillae or the
tectorial membranes, we cannot come to any definite
conclusions regarding their properties. However, the
available morphological and functional data allow for some
hypotheses.
The most conspicuous functional characteristic of the
amphibian papilla is its tonotopic organization (Lewis
et al. 1982). Rostral to the tectorial curtain, the hair-cell
orientation is essentially parallel to the tonotopic axis. In
this low-frequency region of the amphibian papilla, the
tectorial membrane apparently moves in a rostro-caudal
direction. In contrast, the hair-bundle orientation suggests
that the tectorial-membrane motion is perpendicular to the
tonotopic axis in the high-frequency, caudal region of the
papilla. The tectorial membrane’s caudal end, therefore,
appears to vibrate in a markedly different direction than its
rostral end.
In the low-frequency region of the amphibian papilla,
the hair cells display electrical tuning. The tuning proper-
ties of the hair cells parallel the tonotopic organization are
measured from the afferent nerve fibers (Pitchford and
Ashmore 1987). This strongly suggests that the tuning
characteristics of the nerve fibers are primarily determined
by the electrical hair-cell resonances. The auditory nerve-
fiber recordings reflect the presence of high-order filtering
(Lewis 1984), whereas hair cells essentially function as
second-order resonances. It is, therefore, likely that cou-
pling between the hair cells shapes the frequency responses
in the nerve fibers. Such coupling may be mechanical, for
example, by the tectorial membrane, or electrical, or a
combination of mechanical and electrical.
Hair cells in the high-frequency, caudal region do not
display any electrical resonance (Smotherman and Narins
1999). This implies that the frequency selectivity must be
based on mechanical tuning, probably by the tectorial
membrane. The caudal region of the amphibian papilla
shares some notable characteristics with the mammalian
cochlea (see also Lewis 1981):
1. the papilla is elongated, and it exhibits a tonotopic
gradient along the long axis;
2. the orientation of the hair cells is perpendicular to the
tonotopic axis, indicating that the hair cells are
stimulated most efficiently by a deflection perpendic-
ular to the tonotopic axis;
3. frequency selectivity, very probably, relies on mecha-
nical tuning;
4. frequency selectivity is similar, with Q
10dB
-values
ranging from 0.8 to 2.2; and
5. both spontaneous and distortion product otoacoustic
emissions are generated. These emissions are physio-
logically vulnerable.
The presence of spontaneous otoacoustic emissions shows
that at least part of the amphibian papilla’s caudal
extension functions as an active hearing organ. In this
respect it is similar to the mammalian cochlea and other
vertebrate hearing organs (Lewis and Narins 1999). One
active mechanism in the mammalian cochlea is the prestin-
mediated active somatic length changes in the outer hair
cells (Brownell et al. 1985; Yost 2000; Zheng et al. 2000;
Liberman et al. 2002; Dallos 2003). However, this mech-
anism is probably exclusively present in mammalian outer
hair cells. Active hair bundle movements have been
reported as an alternative active mechanism in anuran
saccular hair cells (Martin and Hudspeth 1999; Martin
et al. 2003; Bozovic and Hudspeth 2003); this mechanism
may be present in the auditory organs as well. Although the
fundamental active mechanism may differ between species,
the functional result seems to be very similar across
vertebrates: high auditory sensitivity and good frequency
selectivity (Manley 2000).
The basilar papilla seems to function in a much simpler
manner. Both neural recordings and otoacoustic emission
measurements suggest that it functions as a single auditory
filter. Since the hair cells in the basilar papilla are unlikely
to be electrically tuned, its frequency selectivity most
likely results from mechanical tuning, probably via the
tectorial membrane.
The basilar papilla is remarkable in that no spontaneous
otoacoustic emissions have been recorded in its frequency
range. The absence of such emissions can either be caused
by the fact that they are not generated within the papilla, or
by the fact that the transmission of such emissions to the
tympanic membrane is inhibited. However, distortion
product otoacoustic emissions can be recorded in this range
(e.g., Van Dijk and Manley 2001). This implies that the
outward transmission is not inhibited, and therefore that
J Comp Physiol A (2008) 194:417–428 425
123
spontaneous emissions are most likely not generated within
the basilar papilla.
Furthermore, the amplitude of the basilar papilla’s
distortion product otoacoustic emissions depends less on
temperature than that of the amphibian papilla’s (Me-
enderink and Van Dijk 2006). Also, emissions from the
basilar papilla are less sensitive to the disruption of
oxygen supply (Van Dijk et al. 2003). Apparently,
emissions from the basilar papilla are relatively inde-
pendent of the metabolic rate, and therefore, it has been
suggested that the basilar papilla is not an active hearing
organ (Vassilakis et al. 2004; Van Dijk and Meenderink
2006).
In conclusion, the frog inner ear takes an exceptional
place among the hearing organs of terrestrial vertebrates. It
includes two auditory end organs, which both lack the
basilar membrane present in every other terrestrial verte-
brate species. Instead the hair cells are embedded in a
relatively stiff structure. They are stimulated by the motion
of the tectorial membrane. Although the basilar and
amphibian papilla are similar in this respect, they appear to
function by different mechanisms. In fact, even within the
amphibian papilla two distinctly different functional
regions can be identified. The low-frequency portion, ros-
tral to the tectorial curtain, contains hair cells that exhibit
electrical tuning. The hair cells are most sensitive to
deflection along the tonotopic axis, thus this is presumably
the tectorial membrane’s direction of vibration. By con-
trast, the region caudal to the tectorial curtain shows more
similarities to, for example, the mammalian cochlea: the
hair cell orientation is perpendicular to the tonotopic axis,
and the presence of spontaneous otoacoustic emissions
suggests that it functions as an active hearing organ.
Finally, the basilar papilla is yet different: it appears to
function as a single passive auditory filter. Thus the frog
inner ear includes two auditory end organs with three
functional regions.
Acknowledgments We would like to thank Dr. JEC Wiersinga-Post
for her comments on an earlier version of the manuscript. This study
was supported by the Heinsius Houbolt Foundation and the Nether-
lands Organisation for Scientific Research, and is part of the research
program of our department: Communication through Hearing and
Speech. Previously unpublished data described in this paper were
obtained in experiments conducted in compliance with the ‘Princi-
ples of animal care’’, publication No. 86-23, revised 1985 of the
National Institute of Health, and with the current legislation, at the
time of the experiments, of the country in which they were conducted
(The Netherlands).
Open Access This article is distributed under the terms of the
Creative Commons Attribution Noncommercial License which
permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are
credited.
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... Males typically congregate in flooded areas, attracting females with advertisement vocalizations emitted from inside burrows, where amplexus takes place. Females leave burrows after pairing and males provide parental care to the endotrophic tadpoles ( Formas & Vera, 1980;Penna & Veloso, 1990;Úbeda & Nuñez, 2006;Penna & Márquez, 2007). This genus is divided into two main groups ( Formas, 1992), differing in their vocalizations: species of the Roseus group emit calls with a complex harmonic structure and with frequency modulations, and species of the Vertebralis group produce vocalizations containing amplitude modulations and sidebands ( Penna & Veloso, 1990;Formas, 1991Formas, , 1992Penna & Solís, 1998;Márquez et al., 2005;Opazo et al., 2009). ...
... Species belonging to these two groups have been reported to respond with different behavioural strategies to interference from natural abiotic noises occurring in their native environment ( Penna, Pottstock & Velásquez, 2005;Penna & Hamilton-West, 2007). Two representative Eupsophus species that can be found breeding at the same time and location are Eupsophus roseus ( Duméril & Bibron, 1841) (geographic range from 38°S to 40°S) and Eupsophus vertebralis ( Grandison, 1961) (geographic range from 40°S to 44°S), from the Roseus and Vertebralis group, respectively ( Formas & Vera, 1980;Veloso et al., 2010). The fundamental frequency (346-1019 Hz) of the call of E. roseus has lower energy than the second (875-1429 Hz) and third (1194-2167 Hz) harmonics, and the dominant frequency corresponds either to the second or third harmonic ( Márquez et al., 2005). ...
... These two regions presumably correspond to the input of the amphibian papilla and the basilar papilla, the auditory organs of the inner ear, tuned to low and high frequencies, respectively (e.g. Purgue & Narins, 2000;Schoffelen, Segenhout & van Dijk, 2008). In contrast with other anuran species, such as Physalaemus pustulosus (Cope, 1864), in which two different spectral components of advertisement vocalization match the low-and high-frequency range of enhanced auditory sensitivity ( Wilczynski et al., 2001), the most important frequencies of advertisement vocalizations of E. roseus are restricted to the HFR of enhanced sensitivity of females. ...
Article
The matched filter hypothesis proposes that the tuning of females' auditory sensitivity matches the spectral energy distribution of males' signals. Such correspondence is expected to arise over evolutionary time, as it promotes conspecific information transfer and reduces interference from other sound sources. Our main objective was to determine the correspondence between the acoustic sensitivity of female frogs of Eupsophus roseus and the spectral characteristics of advertisement vocalizations produced by conspecific males. We also aimed to determine how auditory sensitivity is related to the characteristics of background noise. We analysed data on the auditory sensitivity of E. roseus females, and recordings of conspecific male vocalizations and of the acoustic environment during the breeding period of this species. Our results indicate a concordance between the auditory sensitivity of females and call spectra that would provide an appropriate detection of these signals. In addition, this matching is large relative to the correspondence between auditory sensitivity with the spectra of the abiotic and biotic background noise, with the last component being associated with calls of the related species Eupsophus vertebralis. This may be an adaptation of receivers confronting sound interference, which improves the capability of E. roseus to communicate sexually by means of acoustic signals. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 814–827.
... Crickets are part of the prey spectrum of wild anurans (Freed, 1982;Mahon and Johnson, 2007), and House Crickets are used commonly as prey in studies on food preferences and prey capture behavior in anurans (Roster et al., 1995;Taylor, 2001). Crickets use songs to attract mates (Gerhardt and Huber, 2002), and a variety of auditory eavesdroppers take advantage of these songs (Sakaluk and Belwood, 1984;Zuk et al., 2006); the frequencies of cricket songs (Riede, 1998) overlap broadly with the anuran hearing range (Schoffelen et al., 2008). For example, the carrier frequency of our House Cricket song was 4.6 kHz, and the Green Treefrog hearing range extends from 0.3 to 5.4 kHz (Moss and Simmons, 1986). ...
... Most foraging in frogs is visually mediated (Ingle, 1968;Ewert, 1987;Freed, 1988;Buchanan, 1998); yet, it seems intuitive that they might take advantage of their highly developed auditory system (Schoffelen et al., 2008) to aid in prey acquisition. Studies investigating the importance of anuran hearing outside the contexts of mate choice are rare, however, and there is mixed support for the use of hearing in other behavioral contexts. ...
Article
Full-text available
Efficient foraging may be facilitated by attending to the signals produced by potential prey items. Such predatory eavesdropping is taxonomically widespread, yet there is currently a dearth of information for amphibians. Anuran amphibians, with their highly developed auditory system and robust phonotaxis toward advertisement calls when searching for mates, seem predisposed to use this hearing capability in other behavioral contexts such as foraging. We conducted playback experiments to test whether Green Treefrogs (Hyla cinerea) eavesdrop on sexual signals of prey (House Cricket [Achaeta domesticus] song), or whether the presentation of acoustic prey stimuli in addition to a live cricket improved prey localization. We found that frogs did not use acoustic prey signals to guide their foraging movements. Frogs were not indifferent to acoustic stimuli, however, because they moved away from the sound source in some treatments.
... The hair cells in the low-frequency (rostral) patch are probably electrically tuned, whereas those in the caudal extension with higher characteristic frequencies appear not to be electrically tuned Narins, 1999, 2000). Instead, the frequency selectivity here appears to be generated by micromechanical interactions between hair cells and the tectorial membrane including active processes indicated by the presence of spontaneous otoacoustic emissions (review in Schoffelen et al., 2008). The spontaneous emissions are probably caused by active bundle oscillations caused by fast adaptation mechanisms in the hair cell and are found in both saccular and amphibian papilla hair cells (review in Hudspeth et al., 2000). ...
... The high-frequency hearing organ, the basilar papilla, is in many respects simpler than the amphibian papilla and contains fewer hair cells. The hair cells are also covered by a tectorial membrane but generally have the same characteristic frequency and do not show spontaneous otoacoustic emissions (Schoffelen et al., 2008). The characteristic frequency of the cells varies among species, generally ranging from 1500 Hz to above 4 kHz, and is usually tuned to the high-frequency part of the advertisement call (Lewis and Narins, 1999). ...
Chapter
The last several decades of research have seen a burgeoning of data on the morphology, physiology, and evolutionary history of vertebrate auditory organs. This chapter briefly describes the status of our understanding of ear structure and function and their origins in fish, which hear using their vestibular epithelia, and land vertebrates that early evolved dedicated hearing structures. The various major lineages of land vertebrates—amphibians, lepidosaurs, archosaurs, and mammals—each have unique hearing organs. From humble beginnings as a small epithelium in their common ancestor, each lineage evolved specialized hair-cell populations and divisions of labor that led to highly sensitive and frequency-selective hearing. This chapter covers the origins, morphology, and physiological characteristics of the ears of all major groups.
... The inner ear of the American bullfrog contains three auditory organs: the amphibian papilla (AP), the basilar papilla (BP), and the sacculus (S). The AP receives acoustic stimuli within a frequency range of 100 Hz-1250 Hz, while the BP covers the higher portion of the auditory frequency range from about 1.2 kHz to 4 kHz [23]. The sacculus is a mixed-function organ which is most sensitive to low-frequency sounds (120 Hz ± 24 Hz) and seismic sensation [24,25]; however, none of these investigations have focused on prestin and electromotility. ...
Article
Full-text available
The prestin-based active process in the mammalian outer hair cells (OHCs) is believed to play a crucial role in auditory signal amplification in the cochlea. Prestin belongs to an anion transporter family (SLC26A). It is densely expressed in the OHC lateral plasma membrane and functions as a voltage-dependent motor protein. Analog genes can be found in the genome of nonmammalian species, but their functions in hearing are poorly understood. In the present study, we used the gerbil prestin sequence as a template and identified an analog gene in the bullfrog genome. We expressed the gene in a stable cell line (HEK293T) and performed patch-clamp recording. We found that these cells exhibited prominent nonlinear capacitance (NLC), a widely accepted assay for prestin functioning as a motor protein. Upon close examination, the key parameters of this NLC are comparable to that conferred by the gerbil prestin, and nontransfected cells failed to display NLC. Lastly, we performed patch-clamp recording in HCs of all three hearing organs in bullfrog. HCs in both the sacculus and the amphibian papilla exhibited a capacitance profile that is similar to NLC while HCs in the basilar papilla showed no sign of NLC. Whether or not this NLC-like capacitance change is involved in auditory signal amplification certainly requires further examination; our results represent the first and necessary step in revealing possible roles of prestin in the active hearing processes found in many nonmammalian species.
... Treefrogs detect sounds in their environment using two different hearing organs, the basilar papilla and the amphibian papilla (Schoffelen et al. 2008). The basilar papilla functions independently of temperature, as it appears to be mechanically tuned via the tectorial 1018 membrane. ...
Article
Males of many animal species produce conspicuous signals to attract mates; male treefrogs produce loud and persistent acoustic signals called advertisement calls. Frogs face an interesting challenge in that temperature can differentially impact signal production and perception, leading to a mismatch between sender and receiver. For instance, female Green Treefrogs (Hyla cinerea) exhibit temperature-sensitive preferences for the frequency of the advertisement call, potentially resulting in interspecific hybridization at low temperatures. Considering climate predictions by the Intergovernmental Panel on Climate Change, we investigated whether, and by how much, temperature modifies female preferences for natural variation in spectral properties of male advertisement calls. The mate-choice preferences of the Gray Treefrog (H. versicolor) have been extensively studied; females prefer calls with standard bimodal frequency peaks of 1100 and 2200 Hz over calls with higher and lower frequencies. These preferences were determined at 20° C, but the dominant frequency of calls is positively correlated with temperature. Using two-speaker choice experiments, we tested the hypothesis that acoustic preferences of female H. versicolor for the frequency of male advertisement calls vary based on ambient temperatures (15, 20 and 25° C). We found that female preferences based upon frequency are, at best, only moderately temperature dependent. We discuss the possible neurophysiological basis for the seeming lack of temperature coupling in this aspect of the Gray Treefrog communication system, and conclude that mate-choice decisions based on frequency will not be significantly impacted by modest (2° C) changes in environmental temperatures.
... Given their highly developed auditory system (Schoffelen et al. 2008), and the robust phonotaxis towards advertisement calls when searching for mates (Ryan 2001, Gerhardt and Huber 2002, Wells 2007, it seems intuitive that anurans might co-opt their hearing capability for use in other behavioral contexts. Yet, studies investigating its use for foraging (Taylor 2001;Höbel et al. 2014) or risk avoidance (i.e., Leary and Razafindratsita 1998;Schwartz et al. 2000;Grafe et al. 2002; Bernal et al. 2007) are relatively rare, as are studies investigating anuran social information use (but see Lea et al. 2002;Swanson et al. 2007;Buxton et al. 2015). ...
Article
Full-text available
To decide efficiently where to forage, rest or breed, animals need information about their environment, which they may gather by monitoring the behavior of others. For example, attending to the signals of conspecifics or heterospecifics with similar habitat requirements may facilitate habitat choice. Such social information use seems taxonomically widespread, yet there is currently a dearth of information for amphibians. Anuran amphibians, with their highly developed auditory system and robust phonotaxis towards advertisement calls when searching for mates seem predisposed to use this hearing capability in other behavioral contexts. We conducted playback experiments to test whether anurans exploit acoustic signals in a non-reproductive context. In our experiments female Green Treefrogs did not show phonotaxis to signals associated with the presence of other frogs, and the orientation and speed of their movement was not different from animals randomly moving inside a silent arena. Previous studies documenting social information use in anurans have tested reproductively active frogs during the breeding season. By contrast, our study examined non-reproductive animals, and these did not approach social signals. We propose two non-exclusive hypotheses for this observed difference in phonotaxis behavior: (1) attending to social signals is restricted to ecologically most relevant time periods in a frogs life (i.e., finding breeding sites during the mating season), or (2) the ability of acoustic signals to stimulate the auditory system may be influenced by hormone levels regulating the reproductive state.
... The amphibian inner ear is comprised of 5 vestibular end-organs, two auditory end organs and one acoustico-vestibular sacculus that function similarly to the mammalian inner ear. In fact, the auditory organs detect frequencies in the same range as the mammalian cochlea (Elepfandt et al., 2000;Schoffelen et al., 2008;Van Dijk et al., 2011). Thus, novel genes in the Xenopus Six1 pathway are likely to be highly relevant to human ear development and related congenital disorders. ...
Article
Full-text available
Congenital hearing loss is an important clinical problem because, without early intervention, affected children do not properly acquire language and consequently have difficulties developing social skills. Although most newborns in the US are screened for hearing deficits, even earlier diagnosis can be made with prenatal genetic screening. Genetic screening that identifies the relevant mutated gene can also warn about potential congenital defects in organs not related to hearing. We will discuss efforts to identify new candidate genes that underlie the Branchiootorenal spectrum disorders in which affected children have hearing deficits and are also at risk for kidney defects. Mutations in two genes, SIX1 and EYA1, have been identified in about half of the patients tested. To uncover new candidate genes, we have used the aquatic animal model, Xenopus laevis, to identify genes that are part of the developmental genetic pathway of Six1 during otic and kidney development. We have already identified a large number of potential Six1 transcriptional targets and candidate co-factor proteins that are expressed at the right time and in the correct tissues to interact with Six1 during development. We discuss the advantages of using this system for gene discovery in a human congenital hearing loss syndrome. Copyright © 2015. Published by Elsevier Inc.
Article
Mutations in SIX1 and in its co-factor, EYA1, underlie Branchiootorenal Spectrum disorder (BOS), which is characterized by variable branchial arch, otic and kidney malformations. However, mutations in these two genes are identified in only half of patients. We screened for other potential co-factors, and herein characterize one of them, Pa2G4 (aka Ebp1/Plfap). In human embryonic kidney cells, Pa2G4 binds to Six1 and interferes with the Six1-Eya1 complex. In Xenopus embryos, knock-down of Pa2G4 leads to down-regulation of neural border zone, neural crest and cranial placode genes, and concomitant expansion of neural plate genes. Gain-of-function leads to a broader neural border zone, expanded neural crest and altered cranial placode domains. In loss- of-function assays, the later developing otocyst is reduced in size, which impacts gene expression. In contrast, the size of the otocyst in gain-of-function assays is not changed but the expression domains of several otocyst genes are reduced. Together these findings establish an interaction between Pa2G4 and Six1, and demonstrate that it has an important role in the development of tissues affected in BOS. Thereby, we suggest that pa2g4 is a potential candidate gene for BOS.
Article
The frog's basilar papilla is a useful study object for cochlear mechanics, because of it's relatively simple anatomy and functionality. We investigated the displacement amplitudes of the basilar papilla's tectorial membrane in response to stimulation of the oval window at various frequencies within the auditory range of the Northern leopard frog. From our measurement data we find that the tectorial membrane exhibits a frequency selective response. The peak response was found to occur at 1500Hz in correspondence with known data for the response of auditory nerve fibers from the organ. From these data we conclude that mechanical tuning contributes significantly to the frequency selectivity of the frog's basilar papilla
Article
Full-text available
The activity of auditory afferent fibers depends strongly on the frequency of stimulation. Although the bullfrog's amphibian papilla lacks the flexible basilar membrane that effects tuning in mammals, its afferents display comparable frequency selectivity. Seeking additional mechanisms of tuning in this organ, we monitored the synaptic output of hair cells by measuring changes in their membrane capacitance during sinusoidal electrical stimulation at various frequencies. Using perforated-patch recordings, we found that individual hair cells displayed frequency selectivity in synaptic exocytosis within the frequency range sensed by the amphibian papilla. Moreover, each cell's tuning varied in accordance with its tonotopic position. Using confocal imaging, we observed a tonotopic gradient in the concentration of proteinaceous Ca(2+) buffers. A model for synaptic release suggests that this gradient maintains the sharpness of tuning. We conclude that hair cells of the amphibian papilla use synaptic tuning as an additional mechanism for sharpening their frequency selectivity.
Article
Full-text available
We present seismic and auditory frequency tuning curves of individual bullfrog, Rana catesbeiana, saccular and amphibian papilla axons that responded to both seismic and auditory stimuli. In this study we found: 1) most saccular axons respond well to auditory stimuli with moderate signal strength (50-70 dB SPL) as well as to seismic stimuli; 2) most amphibian papilla axons respond well to seismic stimuli as well as to auditory stimuli, and their seismic sensitivities are comparable to those of saccular axons (responding to sinusoidal stimuli with peak accelerations in the range 0.001 to 0.1 cm/s2); 3) the responses to both seismic and auditory stimuli from both saccule and amphibian papilla are tuned, i.e. the strength of the response varies with the frequency of the stimulus; and this tuning is clearly not the result of second order resonance; 4) in individual axons the tuning properties for seismic stimuli often are not the same as those for auditory stimuli, a fact that may provide clues about how the stimulus signal energy is transferred to the hair cells in each case.
Article
The vertebrate ear is highly nonlinear. This is rather surprising since its vibrational amplitudes are so minute in response to normal sound pressures. Generally, one might expect a stable mechanical system to respond linearly when disturbed slightly from its resting state. Thus the nonlinear properties of the peripheral auditory system are of considerable interest inasmuch as they can provide valuable insight into the underlying transduction process in the ear. The two most prominent nonlinear properties are inter-modulation distortion and two-tone suppression. Their characteristics have been studied extensively in the mammalian auditory system by a number of investigators. To provide a comparative view, a series of electrophysiological experiments were conducted in order to determine the nonlinear behavior of the anuran’s peripheral auditory system. The results have interesting implications regarding the origin of nonlinearities, as well as the mechanical basis for frequency analysis, in the vertebrate inner ear in general. Before presenting these findings, several relevant studies of nonlinearities in the mammalian auditory system are summarized, followed by a brief review of the anatomy of the anuran’s ear.
Article
The inner ear of frogs holds two papillae specialized in detecting airborne sound, the amphibian papilla (AP) and the basilar papilla (BP). We measured input–output (I/O) curves of distortion product otoacoustic emissions (DPOAEs) from both papillae, and compared their properties. As in other vertebrates, DPOAE I/O curves showed two distinct segments, separated by a notch or kneepoint. The slope of the low-level segment was conspicuously different between the AP and the BP. For DPOAE I/O curves from the AP, slopes were ⩽1 dB/dB, similar to what is found in mammals, birds and some lizards. For DPOAE I/O curves from the BP these slopes were much steeper (≈2 dB/dB). Slopes found at high stimulus levels were similar in the AP and the BP (≈2 dB/dB).This quantitative difference between the low-level slopes for DPOAEs from the AP and the BP may signify the involvement of different mechanisms in low-level DPOAE generation for the two papillae, respectively.
Conference Paper
By comparing the range of emission frequencies with that of neural characteristic frequencies of the amphibian and basilar papillae, the emission generation site may be inferred. Spontaneous otoacoustic emissions in the amphibian car seem to originate from the amphibian papilla. In contrast, distortion product otoacoustic emission are presumably generated by both the amphibian and the basilar papillae. Distortion products from the amphibian papilla are very sensitive to ischemia; distortion products from the basilar papilla are less sensitive. These results suggest that the basilar papilla may not include an active amplifier. In support of this hypothesis, we show that distortion products from the basilar papilla show only a weak temperature dependence. These emissions are possibly independent of metabolic rate. The basilar papilla in frogs may be the only passive vertebrate hearing organ. In contrast, emissions from the amphibian papilla are clearly temperature dependent, consistent with active auditory processing.
Article
The spectro-temporal receptive field [Hear. Res 5 (1981) 147; IEEE Trans BME 15 (1993) 177] provides an explicit image of the spectral and temporal aspects of the responsiveness of a primary auditory afferent axon. It exhibits the net effects of the competition between excitatory and inhibitory (or suppressive) phenomena. In this paper, we introduce a method for derivation of the spectro-temporal receptive field directly from a second-order Wiener kernel (produced by second-order reverse correlation between spike responses and broad-band white-noise stimulus); and we expand the concept of the spectro-temporal receptive field by applying the new method not only to the second-order kernel itself, but also to its excitatory and inhibitory subkernels. This produces separate spectro-temporal images of the excitatory and inhibitory phenomena putatively underlying the competition. Applied, in simulations, to models with known underlying excitatory and suppressive tuning and timing properties, the method successfully extracted a faithful image of those properties for excitation and one for inhibition. Applied to three auditory axons from the frog, it produced images consistent with previously published physiology. : 2003 Elsevier B.V. All rights reserved.
Chapter
According to current classification, the living amphibians are distributed among three orders—Caudata (newts and salamanders, or urodeles), Gymnophiona (caecilians), and Anura (frogs and toads)—which often are grouped in a single subclass—Lissamphibia. A current summary of the biology of the Lissamphibia is found in Duellman and Trueb (1994). Among the morphological features common to the three orders of Lissamphibia, but lacking in fish, are four evidently related to acoustic sensing (see Bolt and Lombard 1992; Fritzsch 1992 for recent reviews): (1) a hole (the oval window) in the bony wall of the otic capsule; (2) the insertion of one or two movable skeletal elements, the columella and the operculum, into that hole from its lateral side; (3) a periotic labyrinth, part of which projects into the hole from its medial side; and (4) two extraordinarily thin membranes (contact membranes), comprising locally fused epithelial linings of the periotic and otic labyrinths, each contact membrane forming part of the wall of a separate papillar recess in the otic labyrinth. The two papillae themselves may be homologues of two sensors found in fish—the macula neglecta and the basilar papilla. In amphibians, the putative homologue of the macula neglecta is called the amphibian papilla. Among fish, the basilar papilla has been found only in the coelacanth fish, Latimeria (Fritzsch 1987).