Frog Auditory System: The Inner Ear
by David D. Olmsted (Copyright - 1998, 2006. Free to use for personal and
Last Revised October 28, 2006
Overview of the Frog's Auditory System
The regions in the brain involved in processing auditory information are shown
in figures 1 and 2. Figure 1 shows the main information flows while figure 2 shows
where these centers are located in the brain. Notice that the frog's auditory system
does not include the forebrain. The torus semicircularis (TS) is the primary
convergent point while the thalamus (C and P) is the secondary convergent
point. The torus semicircularis also receives inputs from the tactile system
(Comer and Grobstein - 1981b).
Flow Chart of the Main Ascending Auditory Pathways in the Frog. (Feng, et al - 1990)
The Locations and Sizes of the Auditory Centers in the Frog Brain (Top View). (Mudry, et al - 1977)
A dual mode auditory discrimination strategy
is needed when a female frog approaches a pond surrounded by a multitude of calling
males. The calls all merge together such that any temporal characteristics of individual
calls are hidden until the female gets suffeciently close to a calling male. Consequently,
only the frequency and intensity components of their calls can initially be characterized.
The frequency and intensity parameters are characterized by the dorsal medullary
nucleus (DMN) and the superior olivary nucleus (SON). The torus semicircularis is
where temporal pattern information is initially characterized just as it is in the
tactile system. Background context of the temporal pattern information is accomplished
by the thalamus.
The dorsal medullary nucleus (DMN) is a simpler analog to the cochlear
nucleus in mammals while the torus is a simpler analog to the inferior colliculus.
The dorsal medullary nucleus (DMN) receives inputs from the ear via the 8th nerve
and from the dorsal medullary nucleus on the opposite side of the brain. Here is
where the differences in sound intensity between the two ears must be characterized
and amplified. Such a characterization can not be done further downstream
since additional noise and time delays would tend to corrupt the sensory signals
degrading localization performance.
Not shown in figure 1 are the descending
connections. In general each auditory nucleus sends descending neural fibers back
to each of the two nuclei just below itself (Feng -1986a,b: Hall and Feng
The Frog's Ear Structure
A cross-section of the frog's ear is
shown below in figure 3 with bone shown in black. Sound enters the ear via the tympanum
located at skin level behind the eyes which is the analog of the mammalian ear drum.
The tympanum vibrates back and forth pushing and pulling the columella bone against
the fluid filled sacks of the inner ear. This sloshes the fluid back and forth within
the inner ear tubes which house the two auditory sensory structures called
the amphibian and basiler papillas. This sloshing fluid bends the sensory hairs
along one axis so that they can trigger neural signals which travel to the rest
of the brain via the eighth nerve. The Round Window at the end of the inner ear
is another membrane having the purpose of "giving way" so as to allow fluid sloshing
to occur. The muscles are thought to freeze the motion of the the various
bones so as to protect the ear from loud noises. When a frog is exposed to
extremely loud sounds at 165 dB SPL for up to an hour no ear damage occurs (Capranica
and Moffat - 1983, page 711)
Cross-Section of the Frog Ear. (Wilczynski and Capranica - 1984)
The inner ear of the frog like that of mammals generates
a spontaneous sound called an otoacoustic emission. In humans this causes the “sound
of the sea” when one holds up a sea shell to an ear. In frogs this otoacoustic emission
occurs at two frequencies as shown in figure 4 which varies according to the temperature
of the animal.
Spontaneous Otoacoustic Emissions in the Inner Ear of the Frog Rana esculenta. (Long, van Dijk, and Wit - 1996)
The tympanum being similar to a drum has a natural band pass frequency
range. The band pass frequency range for tympanums in four adult Hyla cinerea
frogs is from 200 to 5,000 Hz as shown in figure 5 (although the range probably
extends lower). Compare this to the human ear which can hear frequencies ranging
from 20 to 18,000 Hz.
Band Pass Characteristics of the Frog Tympanum. (Wilczynski and Capranica - 1984)
The Auditory Sensors
Amphibians have two auditory sensory
structures - the amphibian papilla sensitive to low frequencies between 100 and
900 Hz and the basilar papilla sensitive to higher frequencies (Feng, Narins,
and Capranica - 1975 but first proposed by Frishkopf and Geisler - 1966).
The basilar papilla shown in figure 6 is located in tube off of the saccule. It
has on average 60 sensory cells tuned to detect frequencies greater than 1000
Hz. These sensory cells are activated by the bending of hairs protruding from their
surfaces and they are formed into longitudinal rows lining the bottom 1/4 circumference
of the tube (Geisler, et al - 1964). In smaller frogs like Hyla arborea or
Bombina bombina the hairs may number as few as 14 (reported in Wilczynski
and Capranica - 1984). A membrane structure fills the bottom half of the tube
which seems to have two purposes: the first which is to form individual fluid filled
channels for each row of sensory hairs while the second is to hold a thick
jelly-like substance within these rows which is better able to push the sensory
Cross-Section of the Basilar Papilla in the Bull Frog Rana catesbeiana. (Geisler, Bergeijk, and Frishkopf - 1964)
The sensory cells have no axon of their own. Instead they send their
signals to the dorsal medullary nucleus via fibers originating from neural cells
located in the posterior eighth nerve ganglion. The output nerve of the basilar
papilla is one of four branchlets of the posterior branch of the eighth cranial
nerve and it averages 350 fibers. (Geisler, et al - 1964). Since each fiber
connects to only one sensory cell (Lewis, et al - 1982) this means that each
hair sensory cell triggers signals in an of average of 6 fibers for a redundancy
factor of 6. Fiber tracing studies also show that each fiber is unique
to each sensory hair cell meaning that each fiber does not branch to multiple
sensory cells (Lewis, et al - 1982a).
In contrast to the high frequency detection
of the basilar papilla, the amphibian papilla is sensitive to the lower frequencies.
It is an "S" shaped tube which is tonotopically organized from 140 to 940
Hz in Rana catesbeiana with the lowest frequencies at one end and the highest
frequencies at the other end (Lewis, et al - 1982b). No such tonotropy
has ever been found in the basilar papilla. It averages 600 sensory hair cells
in the bullfrog Rana catesbeiana which is 10 times more then the basilar papilla
(Geisler, et al - 1964). These hairs are covered with a fine membrane.
The sensory hair cells project their signals on fibers originating in posterior
eighth nerve ganglion via its own branchlet of the posterior branch of the
eighth sensory nerve. This branchlet averages 1010 fibers (Geisler, et al
- 1964) so each sensory cell could send its signal on one or two fibers. Yet
each fiber branches to connect from 1 to 15 sensory cells (Lewis, et al -
1982a).The greatest overlapping of sensory cells occurs in the lowest frequency
region (< 300 Hz) ranging from 1 to 15 cells, the middle frequency
region (300 - 600 Hz) is next with overlapping ranging from 1 to 8 cells, while
the highest frequency region (600 - 1000 Hz) has overlapping ranging from 1 to 6.
This seems to indicate that several high frequency sensory cells in the amphibian
papilla are needed to produce the same signal intensity as the lower frequency
sensory cells in the basilar papilla which has no overlapping. This makes sense
since the degree of hair bending is responsible for signal generation and high frequency
sounds with their shorter wavelengths would not be able to push the hair cells as
The nerve which carries information from the inner ear to the brain stem is
the eighth cranial nerve. Near the ear it separates into two main branches,
the posterior branch and the anterior branch as shown in figure 7. The number
of fibers counted in the posterior branch of the eight nerve by Geisler, et al (1964,
page 56) is 2,900 while the number of cells in the posterior eighth nerve
ganglion is 2,600. Of these the auditory system uses 1360 fibers or nearly
half leaving the rest for use by the ground and water vibration signals from the
Lagena (L) and by the head motion signals from the posterior vertical canal
(PVC). The anterior branch of the eighth nerve passes vibration signals from the
sacule and vestibular signals from the other canals and the utricle (Lewis,
et al - 1982a)
Eighth Nerve Innervation of the Ear - Bottom (Ventral) View. (Feng, Narins, and Capranica - 1975)
AVC - anterior vertical canal, AP - amphibian papilla, BP - basilar papilla, HC horizontal canal, L - lagena, OC - otic capsule, PVC - posterior vertical canal, S - sacule, U - utricle, VIII n. gang. - eighth nerve ganglion. Letters show recording locations.
Inputs to the Auditory Sensors
Interestingly, one set of fibers projects
FROM the brain stem TO the auditory sensory hair cells in aquatic frogs (Hellmann
and Fritzsch - 1996) and salamanders (Fritzsch and Wahnschaffe - 1987) but
not in land frogs (Robbins, Bauknight, and Honrubia - 1967). These fibers carry
a signal which is also involved in controlling the responses of the lateral
line system in fish and aquatic amphibians. The lateral line system consists of
sensory hair cells like those found in the inner ear but arranged in rows
on the surface of the skin thus allowing the animal to characterize the flow
of water aound itself. These projections from the brain stem are shown in
figure 8. Notice that the saccule responsible for detecting water and earth born
vibrations receives many inputs while the auditory sensors and others receive only
one but that one seems to contact most if not all of the sensory cells.
Lateral Line Input Fibers to the Inner Ear in the Aquatic Frog Xenopus laevis. (Hellmann and Fritzsch - 1996)
originate from approximately of 11 cells in the medial reticular formation just
above the Superior Olivary nucleus of the aquatic frog Xenopus laevis.
correspond in location to the rostal (headward) group of the lateral line projection
cells. The lateral line cells are located in two groupings along the head to tail
longitudinal axis. The rostal (headward) group averages 6 cells which project to
the head region while the caudal (tailward) group averages 4 cells which project
to the body region. Two of the cells in the rostal group project to both the
lateral line and the inner ear while one of the cells in the caudal group
projects to both the head and body regions.
As suggested by Hellmann and Fritzsch
(1996) these fibers to auditory system are most likely inhibitory since the
projections to the lateral line sensory cells in salamanders are inhibitory (Munz
and Class - 1991) and projections to the the sacule are inhibitory (Sugai
et al - 1992).
Frequency Characteristics of the Auditory Signals
Each neuron fiber
in the posterior branch of the eighth nerve is tuned to a certain frequency.
Figure 9 below gives a representative sample of the tuning curves in
Rana catesbeiana for the three main frequency response groupings or clusters as seen
in the three peaks of figure 10. Tuning curves give the minimum sound
level at each frequency needed to activate
the neuron. Curve 1 in figure 9 has a
Best Excitatory Frequency
(BEF) at 250 Hz, curve 2 at 600 Hz, and curve 3
at 1400 Hz. (Notice the heading above the illustration - who says researchers
don't have a sense of humor!).
Tuning Curves Found in the Eighth Nerve Axons in Rana catesbeiana. (Feng, Narins, and Capranica - 1975)
Histogram of Best Excitatory Frequencies Found in 135 Axons in the Eighth Nerve of Rana catesbeiana. (Feng, Narins, and Capranica - 1975)
In all frogs tested the the lowest frequency detecting neurons which
originate from the amphibian papilla can be inhibited by sounds of another
usually higher frequency. This type of inhibition is called two-tone rate suppression. Figures 11 and 12 show
the characteristics of this inhibition. In figure 11 the solid line has a best
excitatory frequency at 275 Hz. Its signal at 10 dB dB above threshold (the "x")
was totally inhibited by the tones at the loudness level shown by the dotted curve.
The dotted inhibitory curve has a best suppression frequency of 900 Hz. If the intensity of the tone is increased then the threshold of the best suppression frequency increases in proportion to match
it (Capranica and Moffat - 1983, page 717). This inhibition is due to activity from the amphibian papilla neurons since
the inhibition remains
when the nerve branchlet to the basilar papilla is cut (Feng, Narins, and Capranica
- 1975). While most inhibitions are due to higher frequencies some are due to lower
frequencies at least in Rana pipiens (Bendix, Pedemonte, Velluti, and Narins - 1994).
Mammals also exhibit this two-tome rate suppression.
Tuning Curves Found in the Eighth Nerve of Green Treefrog Hyla cinerea. (Capranica and Mofat - 1983)
Histogram of the Best Excitatory Frequencies found in 164 Axons in the Eighth Nerve of Hyla cinerea. (Capranica and Mofat - 1983)
Not only do the eighth nerve
axons have different frequency responses but they also have different response
thresholds as shown at the top (A) of figure 13. Adding broadband noise from 20
to 10,000 Hz as shown at the bottom of figure 15 (B) effectively lowers the
thresholds showing that each sensor sums the energy from all its detectable frequencies.
Notice the variation in the low frequency clusters between the pure tone and noise
samples which is most likely caused by their inhibitory connections.
These samples came from 8 adult frogs. The broadband noise is from 20 to 10,000
Hz. Notice the logarithmic frequency scale which tends to minimize the large
separation between the high frequency cluster and the other clusters.
Thresholds and Best Excitatory Frequencies (BEF) from 177 Eighth Nerve Axons in Hyla cinerea for Both Pure Tones (A) and Broadband Noise (B). (Ehret and Capranica - 1980)
Temporal Characteristics of the Auditory Signals
The axons in the eighth nerve exhibit some low level of
spontaneous activity although reports as to the exact level are contradictory perhaps
due to differing methods of frog preparation. Capranica and Moffat (1983, page 719)
report that in Hyla cinerea
the neurons of the lowest frequency cluster have a spontaneous
firing rate of less than 5 pulses per second. The middle cluster has a spontaneous
firing rate of less than 10 spikes per second while the highest frequency
cluster has a spontaneous firing rate of between 10 to 40 spikes per second. In
contrast Ehret and Capranica (1980, page 3) say this about the eighth nerve
activity in Hyla cinerea:
"The spontaneous activity of almost all fibers was less
than 6 spikes/s with the majority below 1 spike/s. Only 10 fibers of the low
and mid frequency range had spontaneous rates between 6 and 16 spikes/s."
That differing methods of frog preparation are indeed behind this descrepancy is
supported by the findings of Christensen-Dalsgaard, Jorgensen, and Kanneworff (1998)
who allowed their frogs to recover from surgury for one or two days before proceeding
with the neural recordings. Out of 401 auditory neurons recorded in 31 European
grassfrogs (Rana temporaria) they found the median spontaneous activity to
be 8.6 spikes per second with the distribution shown in figure 14. Those neurons
having higher sound intensity thresholds tended to have lower spontaneous activity
while no correlation was found with the neuron's best exitatory frequency.
This is in contrast to what Capranica and Moffat (1983, page 719) found in Hyla cinerea:
As pointed out by Christensen-Dalsgaard, Jorgensen, and Kanneworff in there paper
the higher spontaneous activities seem to appear after the frog has had time
to recover from the trauma of surgery. What causes this neural suppression is unknown."
Spontaneous Auditory Eighth Nerve Fiber Activity in Rana temporaria (Christensen-Dalsgaard, Jorgensen, and Kanneworff - 1998)
Once the threshold has been exceeded increasing sound intensities produce linearly
increasing action potential frequencies as shown in figure 15. The maximum rate
is 220 spikes per second which is on the high side for any brain. Different neurons
have different dynamic ranges for sound intensity detection with more restricted
ranges at the greater frequencies. Still with a minimum range of 60dB more thresholds
exist than is necessary to cover the whole range of 0 to 100 dB indicating
that the thresholds exist for a different purpose. The most likely explanation
is that they exist to implement the cascading threshold strategy for sound
gradient climbing as described on the
Frog Auditory Behavior
Representative Rate Intensity Curves from Eighth Nerve Axons in Hyla cinerea. (Capranica and Moffat - 1983)
The auditory sensor
neurons feeding into the eighth nerve do not habituate to repeated stimulation (Megela
and Capranica - 1983).
The spike rates for the eighth nerve fibers change with temperature
as indicated in figure 16. As all chemical reactions increase with temperature this
is to be expected yet it shows that any decisions made by the frog brain must be
based upon relative competition and not dependent upon absolute thresholds.
Temperature Effects on Neuron Spiking Rates (van Dijk, Lewis and Wit - 1990).
Solid lines connect data from same fiber. Dashed lines also connect points from the same fiber but with the sound stimulus increased by 10 dB.
high spike frequencies are needed both for sound localization and sound pattern
recognition. In regards to sound pattern recognition the action potentials must
be able to follow the temporal characteristics of the various calls as shown below in figure
17. Notice that the pulsed nature of the Rana Pipiens
is captured in
the neuron's response when the data is the summation
of 50 trials. Yet the maximum number range of action potentials is only from 0 to 10. This data also suggests that some sort of temporal summation is needed for sound pattern recognition.
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