NuB502: THE AUDITORY SYSTEM
Bruce L Tempel (bltempel@u.)
These lectures on the auditory system will switch back and forth between structure and
function as we work our way through the system. Thus, we should start by considering the
qualities of physical energy that the system is required to transduce in order to give us
meaningful information about our acoustic environment.
WHAT WE HEAR
Sound, in the form of pressure waves in the environment, is transmitted to the brain via
electrical signals from the cochlea. Sound is composed of pressure waves of molecules in the
medium (air or water). As a vibrating object pushes in one direction the molecules are
compressed in front of it and a relative vacuum is created behind the object (rarefaction). As it
moves in the opposite direction the reverse happens. These pressure waves are propagated
through the medium, spreading as a square of the distance from the source, at a rate determined
by the properties of the medium (density, temperature, pressure, etc.), much like ripples of water
when a stone is dropped in a pond (Figure 1).
Figure 1. Simple pure tone
propagation.
The simplest sound is a pure tone, made by the sinusoidal movement of an object like a
tuning fork. It can be characterized by the amplitude and frequency of the propagating waves,
and the source of the sound. Complex sounds can be thought of (and analyzed as) combinations
of pure tones having differing amplitudes and phase relationships.
Through interactions of neural circuits, two tasks must be performed. First, the spatial
location of the sound source must be determined. Second, the “spectral content” of the sound
pattern must be continuously determined. The frequency and intensity, at any time, represent the
“spectral” content” (or “spectrum”) of sound. The structures and pathways considered most
important for these functions will be briefly outlined below. Where possible we will conjecture
on the functional importance of these structures.
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Three independent parameters of an acoustic stimulus must be considered.
1. Frequency: Defined on the basis of the number of cycles per second of a simple sine wave.
The period of simple sinusoidal wave is 1/frequency. Units: cycles per second (cps) or Hertz
(Hz). The wavelength of a particular frequency component depends on the medium and is
calculated by the period x velocity of sound propagation in the medium. Average “normal”
human range of frequency sensitivity – 20 Hz to 20 kHz. There are very wide species
variations in the frequencies that can be heard. Among vertebrates, mammals, in general, are
high frequency specialists, some hearing above 100 kHz. Complex sounds can be
represented by a Fourier analysis showing the relative contributions of each frequency or
frequency band.
2. Amplitude (or Intensity): Technically, refers to the amount of the displacement from peak
to peak (see Figure 1) in one cycle that the source moves around its equilibrium point. In
practice we measure it as force (pressure) at the object. The intensity range of hearing, from
the softest sound we can detect to the loudest sound we can analyze, is so large, it is not
practical to express it on an equal interval scale. Therefore sound intensity is usually
measured and defined on the basis of relative force, or a ratio scale (in this case log10 scale).
In general the basis (reference level) for this ratio is the force required for human auditory
threshold at 1000 Hz: 0.0002 dynes/cm2.
Intensity units: decibels (dB). X(dB) =20log10
measured pressure
reference pressure
When referenced to human threshold (0.0002 dynes/cm2) amplitudes are noted in dB (SPL),
where SPL = Sound Pressure Level.
The convenient rule of thumb is that every 6 dB increase in measured intensity is equal to
doubling the stimulus energy.
Range of human sensitivity is the astronomical 0 to 120 dB (SPL); i.e., from the softest to the
loudest sound we can deal with, that is a ratio of approximately 1 to 1 billion in pressure.
3. Sound Source: Direction of a sound source is defined on the basis of the origin of the sound
source. Units: degrees azimuth on the horizontal plane (0-360). When sound encounters an
object it can be reflected, absorbed or pass through (or around) the object. The result will
depend on the density of the object, and the size of the object. For practical purposes in air,
sound will pass around objects that are smaller than one wavelength and objects that are
larger than one wavelength will form a barrier, casting a “sound shadow” behind them. This
becomes important for understanding how the brain calculates the position of sound in space.
Consider that the Speed of Sound in air is approximately 340 m/sec.
Wavelength:
1000 Hz = 34 cm
500 Hz = 68 cm
440 Hz (middle C) = 77 cm
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Figure 2: The lower curve shows the minimum
audible sound-pressure level for human subjects as
a function of frequency. The upper curve shows
the upper limits of dynamic range, the intensity at
which sounds are felt or cause discomfort. (After
Durrant, J.D.; Lovrinic, J.H. Introduction to
psychoacoustics. In Durrant, J.D.; Lovrinic, J.H.,
eds. Bases of Hearing Science. 138-169.
Baltimore, Williams & Wilkins, 1984.)
SENSORY SYSTEM GENERIC ORGANIZATION
Figure 3.
PERIPHERAL SPECIALIZIATIONS
1. Outer Ear
Airborne sound waves consist of alternating rarefaction and condensation of airborne
molecules. These relatively large, low force environmental patterns must be converted to high
force, small volume changes at the oval window (Consider a high note [e.g. 1000 Hz]. At
standard atmospheric pressure one cycle is over a foot long. Lower frequencies, for example
those in the speech range, are progressively longer). This task is accomplished by the structures
comprising the external and middle ear.
Figure 4: The external ear, composed
of the pinna and ear canal, protects
the eardrum and directs sound waves
toward it. These elements alter the
acoustic spectrum reaching the
eardrum differentially depending on
the frequency and on the relative
location of a sound source. See
Figure 5: a sound emanating from the
front will be enhanced by as much as
16 dB in the 1.6-10 kHz range at the
eardrum; it can also be reduced by 212 dB at high frequencies.
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Figure 5: The difference between the
sound levels produced at the tympanic
membrane and those produced at the
same point in space with the person
absent is plotted as a function of the
frequency of the constant sound source.
The curve results mainly from ear canal
and pinna resonance. (After Shaw, E.A.G.
Transformation of sound pressure level
from the free field to the eardrum in the
horizontal plane. Acoust. Soc. Am.
56:1848-1861, 1974.)
2. Middle Ear
The impedance mismatch between air and the fluid filled cochlea would result in very little
sound absorption without some mechanism to increase pressure at the oval window.
Calculations suggest that his transmission loss would be on the order of 99.9%, which agrees
well with clinically derived values of 30 dB hearing loss following fenestration of the stapedial
footplate in patients with otosclerosis.
The middle ear ossicles (malleus, incus, stapes) work in concert to provide a mechanical
transformer. (See Figure 6).
Figure 6: The impedance matching
mechanisms of the middle ear.
Both the difference in length
between malleus handle (L1) and
incus long process (L2) and the
much larger ratio of areas of
tympanic membrane (A1) to stapes
footplate (A2) are shown. (After
Abbas, P.J. Physiology of the
auditory system. In Cumming,
C.W., ed. Otolaryngology, Head
and Neck Surgery, 2633-2677, St.
Louis, C.V. Mosby, 1986.)
The malleus attaches to the medial surface of the tympanic membrane and articulates with
the incus. Attached to the other end of the incus is the head of the stapes. The footplate of the
stapes is inserted into the oval window of the cochlea. The transformer action of the middle ear
bones results principally from two factors. First and most important is the ratio between the
sizes of the tympanic membrane and the footplate of the stapes (about 20:1). This ratio means
that the movements of the tympanic membrane will be concentrated on a much smaller area at
the oval window. The second factor is the lever ratio of the ossicular chain. Large movements
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of the tympanic membrane result in smaller, more forceful, movements of the stapes. In all, the
mechanical transformer action of the middle ear produces a gain of approximately 70-100 fold.
Its significance can be clearly appreciated by the fact that the coefficient of sound transmission
from the tympanic membrane to the cochlea is increased from less than 0.1% to over 50%. The
middle ear can be thought of as a “transformer”. It dramatically increases the mechanical energy
focused onto the fluid-filled inner ear, thereby partially alleviating the impedance mismatch
between air and water.
Attached to the ossicles are two small muscles, the tensor tympani and the stapedius. The
tensor tympani attaches to the malleus and the stapedius attaches to the stapes. The trigeminal
nerve innervates the tensor tympani muscle while the facial nerve innervates the stapedius
muscle. Contraction of either muscle decreases sound transmission through the middle ear by
placing increased tension on the middle ear conduction system.
The middle ear muscles respond to a variety of stimuli, the most important of which are
during vocalizations and during moderate to loud acoustic stimulation in either ear. The latter is
the acoustic middle ear reflex, a 3-5 neuron brainstem circuit elicited by stimuli at or above 80
dB above threshold. This reflex culminates in a graded contraction of the middle ear muscles. At
maximal contraction of the stapedius muscle sound transmission is damped by a factor of 0.6-0.7
dB/dB of increased sound pressure at the eardrum. The acoustic middle ear reflex probably
serves several functions: 1. to protect the cochlea from overstimulation; 2. to increase the
dynamic range of hearing; and 3. to reduce masking of high frequencies by low frequency
sounds. Taken together the latter two functions will significantly improve speech discrimination,
especially in noisy environments.
In addition to loud sounds and during vocalizations, contraction of the middle ear muscles
may be activated by nonacoustic exogenous and endogenous stimuli, for example cutaneous
stimulation around the ear or eye. Some individuals can voluntarily contract their middle ear
muscles.
3. The Cochlea
The transduction of mechanical energy to electrochemical neural potentials takes place in
the cochlea (auditory portion of the inner ear). The osseous or periotic cochlea is a bony, fluid
filled tube enclosed within the petrous portion of the temporal bone, and coiled around a conical
pillar of spongy bone called the modiolus. Embedded in the modiolus are the cell bodies of the
spiral ganglion cells, whose axons make up the auditory portion of the eighth nerve. Within the
cochlear duct are three longitudinal chambers (scalae). Fluid motions set up at the oval window
by movement of the stapedial footplate are dissipated at the round window. Between the scala
vestibuli and scala tympani is the scala media, or cochlear duct, containing the auditory receptor,
the Organ of Corti (see conceptual buildup in Figure 7). Lining the lateral wall of the cochlear
duct are the cells of the stria vascularis which maintain the ionic difference between the
perilymph within the scala vestibuli and tympani, and the endolymph within the cochlear duct.
The mammalian cochlea is a three-chambered spiraled tube which is about 34 mm long in
humans and has anywhere between 1.5 and 3.5 turns, depending on the species (2.5 in humans).
The principles of transduction are shown in the following figures. Fluid pressure changes are
initiated by the vibratory pattern of the stapes at the oval window adjacent to the scala vestibuli,
and “released” at the round window. The middle compartment, scala media, contains the Organ
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of Corti and the stria vascularis. The organ of Corti is situated on the basilar membrane and
contains the transduction apparatus, which can be thought of as a repeating structure containing 1
inner hair cell and 3 outer hair cells, plus a complex group of associated support cells and
structures. Hence, the structures shown in Figures 8 and 9 below are repeated all along this tube,
resulting in a single row of inner hair cells (~3,500 in humans) and 3 rows of outer hair cells
(~12,000 in humans). The stria vascularis provides the high potassium concentration and
resulting resting potential (~ +80 mV) of the scala media. This sets up an enormous potential
difference (driving force) of about 150 mV across the apical surfaces of the inner and outer hair
cells.
Figure 7: Drawings showing the fundamental
plan of the cochlea. A: The cochlea
represented as a fluid-filled container with an
elastic membrane (oval and round window
membranes) covering each end. The rigid
wall of the container corresponds to the bony
capsule of the cochlea. B: A driving piston,
the stapes, and a middle elastic membrane the basilar membrane - are added. C: Sensory
(hair) cells with attached nerve fibers are
placed on the basilar membrane, and a hole
(the helicotrema. D: The wall of the cochlea
near the helicotrema is extended; its
mechanical properties varying systematically
with longitudinal position along the
membrane. The sensory cells are
differentiated into inner and outer hair cells.
The auditory nerve fibers shown are radial
fibers that innervate the base of inner hair
cells. A far smaller proportion of fibers (not
shown) branch extensively to innervate outer
hair cells. E: The elongated cochlea is coiled
along its length to arrive at a simplified model
- of the mammalian cochlea.
The actual transduction of mechanical to electrical potentials takes place in the hair cells.
Differential movements of the basilar membrane and the overlying tectorial membrane are
thought to cause minute shearing forces on the hair cell stereocilia bundles. When the bundle
moves in one direction (toward the longest stereocilia) transduction channels are opened,
allowing influx of K+ and Ca++ ions (Figures 10 and 11). Channels close when the bundle is
moved in the opposite direction. The details of this process have been studied in considerable
detail, but are not the subject here. Suffice it to say that the hair cells and supporting structures
are highly specialized for remarkable sensitivity and rapid response properties.
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150 mM K+
+80mV
4 mM K+
0mV
RETICULAR
LAMINA
(tight
junctions)
PERMEABLE
Figure 8: Top: Cross section of cochlear duct. The boundaries of the scala media with the
scala vestibuli and with the scala tympani are Reissner's membrane and the basilar
membrane respectively. Bottom: Organ of Corti showing most important structures and
cell types.
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Figure 9: The cochlea contains the
Organ of Corti, which rests on the
basilar membrane and contains hair
cells that are surrounded by an
elaborate network of supporting
cells. There are two types of hair
cells: inner hair cells and outer hair
cells. The hair cells are innervated
at their bases by afferent fibers.
These nerve fibers have cell bodies
in the spiral ganglion. Efferent
fibers from the central nervous
system synapse on afferent terminals
beneath the inner hair cells and on
the bases of the outer hair cells.
Figure 10: Diagram showing how
an "upward" (toward scala
vestibuli) displacement of the
cochlear partition can create a
shearing force tending to bend hair
cell stereocilia in an excitatory
direction. (After Ryan, A., Dallos,
P. Physiology of the Inner Ear. In
Northern, J.L. ed. Communicative
Disorders: Hearing Loss, 80-101.
Boston. Little, Brown & Co.,
1976.)
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Figure 11: Deflection of the hair
bundle toward the tallest row of
sterocilia opens poorly selective
cationic channels near the
sterocilia tips. A, Influx of
potassium depolarizes the cell. B,
Voltage-sensitive calcium channels
open in turn, permitting C,
neurotransmitter release across the
synapse to the afferent neuron
(After Hudspeth, A.J. The hair
cells of the inner ear. Sci. Am.
248:54-64, 1983.)
Functionally, an extremely important feature of the cochlear duct is that the spectral pattern
of footplate vibration at the oval window is translated into a spatial pattern of basilar membrane
movement ("The cochlea performs a spectral to spatial transformation"). The basilar
membrane is narrowest near the oval window (basal portion) and gradually widens toward the
apex (Figure 12). Due to this fact and the associated changes in stiffness, high frequency sounds
produce maximal displacement of the basilar membrane toward its basal end and progressively
lower frequencies produce maximal movement toward the apex. This translation of acoustic
frequency into a spatial array was first elegantly demonstrated by George von Békésy. (Using
stroboscopic illumination of the basilar membrane von Békésy was able to view its movements
through a microscope. He found that acoustic stimuli produced deflections of the basilar
membrane with a period equal to the stimulating tone and which travel down the cochlear duct in
a wave-like motion (Figure 13). The shape of the "traveling wave", the distance it travels from
the oval window, or base of the cochlea, and the position of maximum deflection are all
dependent on frequency.) High frequencies produce relatively narrow waves that have their
maximum deflection near the oval window and then are rapidly damped. As the frequency of the
stimulating tone is decreased the wave front become progressively broader, the position of
maximum displacement moves apically, and the traveling wave move progressively further down
the cochlear partition. Thus, the cochlea is seen to be a very efficient acoustic spectrum
analyzer, transforming the spectrum of mechanical movements at the oval window into a
spatial array of basilar membrane deflections (Figures 14 - 17).
The hair cells, in line along the basilar membrane, are maximally activated by maximal
deflections of the membrane, thus preserving the tonotopicity. At the base of the hair cells are
found synaptic specializations which are thought to use glutamate as the afferent transmitter.
Very importantly, the general principle of a spatial representation of frequency (tonotopicity),
which is first manifest in the movements of the basilar membrane, is preserved throughout the
entire auditory system and is probably responsible for behavior frequency selectivity.
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Figure 12: The snail-shaped cochlea
is straightened out, and the basilar
membrane is shown as a tapered
ribbon. An instantaneous picture of
the traveling wave is indicated by
the shape of the basilar membrane,
assuming the sound input is a pure
tone. The amplitude of the traveling
wave is grossly exaggerated.
Figure 13: Traveling waves in the
cochlea. The full lines show the pattern
of the deflection of the cochlear partition
at successive instants, as numbered. The
waves are contained within an envelope
which is static (dotted lines). Stimulus
frequency: 200 Hz from von Békésy
(1960, Fig 12.17)
Figure 14: The dimensions of the
basilar membrane change along its
length. In this surface view, the
basilar membrane is shown
diagrammatically as if it were
uncoiled and stretched out flat.
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Figure 15: Plots of data from von
Békésy's experiments on the
mechanics of the basilar membrane
show that the peak amplitude of the
traveling wave occurs at different
points for that these curves reflect
only the overall envelope of motion
of a complex wave along the
basilar membrane.
Figure 16: Schematic of
traveling wave to three
different frequencies. Note
that the envelope is broader
and travels further toward
the apex as the frequency is
lowered. Depicted with
“unrolled” cochlea.
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Figure 17: Frequency organization
of human cochlea.
Von Békésy’s original observations suggested that the traveling wave is very broadly tuned
to frequency, which was in sharp contrast to the very sharp frequency tuning near threshold of
the axons of the cochlear nerve (see below). Von Békésy was studying cadavers and dead
animals. Modern instrumentation, allowing direct visualization of the basilar membrane motion
in live preparations, has shown that at low sound levels the tuning of basilar membrane motion
matches the properties of 8th nerve axons. This sharp tuning is referred to as frequency
specificity and is the result of an active process that enhances response amplitudes at low sound
levels, but progressively this enhancement as sound level is increased - a “compressive
nonlinear” amplification (Figures 18, 19).
Figure 18: Tuning of basilar membrane response. Note
that tuning is much sharper at low intensities than at high
intensities (e.g. 80 dB). Note also that the response is
highly nonlinear at the optimum frequency (14 kHz) but
linear at low frequency (3 kHz).
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Threshold
Amp
Cochlear
Amplifier
Figure 19: Response envelope of
basilar membrane to low level
stimulus at a particular frequency.
Note that contribution of the outer
hair cells (cochlear amplifier)
increases the response selectively
at one place along the basilar
membrane.
Base
Apex
Ganglion
Cells
Auditory
Nerve
4. The Role of Outer Hair Cells
In mammals, there exist two types of hair cells, inner and outer. Their detailed structures,
functions and innervation patterns are quite different (as discussed below) but both convert
mechanical energy into electrical signals. To accomplish this, both depend on stereocilia with
mechanically gated ion channels to open, allowing cations (K+ and Ca++) to enter and depolarize
the cell. The battery powering this process is provided by the relatively high concentration of K+
in the endolymph, establishing an electrochemical gradient with respect to the hair cell and
perilymph.
Figure 20: Inner and outer hair cell. Note
that afferent terminal on inner hair is
contacted by efferent fiber, while efferent
fibers directly contact outer hair cells.
Almost all of the information getting to the brain comes from the inner hair cells via the
spiral ganglion cells. The outer hair cells however, seem to play a critical role in terms of both
the sensitivity and tuning of the cochlea. Figure 18 shows the mechanical tuning of one place
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along the living cochlea. Without the outer hair cells the sharp tuning and high sensitivity (i.e.
response to 20 and 40 dB) are lost.
Most hearing loss is due to loss of outer hair cells. The nonlinearity of this "cochlear
amplifier" can be measured acoustically in the form of otoacoustic emissions - sounds measured
in the ear canal.
Figure 21. Activity in Outer Hair Cells.
Figure 22. Tones emitted in response
to the primary tones, f1 and f2, are
dependent on OHC activity.
5. Neural Innervation of the Hair Cells
The precise pattern of hair cell innervation has been extensively studied during the past two
decades. At the base of the hair cells two types of ending can be recognized. The afferent
endings, opposite the above mentioned synaptic specializations in the hair cells, are the distal
dendrites of the cochlear ganglion cells, whose cell bodies are embedded in the body modiolus
along the length of the cochlea. The second type of ending has synaptic vesicles within the nerve
terminal and can be stained with acetylcholinesterase or choline-acetyltransferase and is
therefore thought to be efferent and presynaptic to the hair cells. These efferent terminals have
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their cell bodies near the superior olivary nuclei of the brainstem and comprise the final
termination of the axons of the olivo-cochlear system.
Figure 23. Innervation of inner and outer hair
cells by spiral ganglion neurons.
The distribution of afferent and efferent endings on the outer and inner hair cells differs
strikingly. The vast majority of spiral ganglion cells (95%) terminate on inner hair cells. Only
about 5% of these afferent fibers cross the tunnel of Corti to receive synaptic connections from
the outer hair cells.
6. Spiral Ganglion Cells and Auditory Nerve
The spiral ganglion cells are distributed within the spiral (Rosenthal's) canal of the modiolus,
along most of the length of the cochlea. (In man there are about 23, 000 spiral ganglion cells).
The distal processes of the ganglion cells (dendrites) pass through the habenula perforata and
become unmyelinated prior to entering the Organ of Corti. The proximal processes (axons) form
the auditory portion of the eighth cranial nerve. After passing through the central core of the
modiolus the axons form the cochlear nerve that travels with the vestibular and facial nerves in
the internal auditory meatus. The axons are myelinated throughout their length. Just before
entering the cranial cavity Schwann cells are replaced by neuroglia cells. Upon entering the
cranium the auditory and vestibular fibers segregate to arrive at their neural targets.
Physiological studies on the response properties of cochlear nerve fibers of experimental
animals (cats and monkeys) show that:
1. Most fibers have a moderate spontaneous activity that appears to be abolished by hair cells
destruction.
2. There is a single excitatory best frequency to which the fibers respond at lowest intensity.
3. The fibers have a simple V- or U-shaped excitatory "tuning curves" surrounding the best
frequency.
4. The fibers display a monotonic increase in firing rate up to a maximal level as the intensity of
the preferred tone is increased and then show a constant or slightly reduced firing rate.
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In addition, the spike train of most fibers that respond best to low frequencies is time locked
to the sinusoid of the stimulating tone so that the intervals between successive spikes tend to be
at the period of the sinusoid or some integer multiple thereof (Figure 27). This latter property is
termed "phase-locking" and is probably important both for low frequency sound localization and
for frequency discrimination at normal listening levels.
Figure 24. Action
potentials (spikes)
recorded in 8th
nerve in response to
various sound
stimuli.
Figure 25: "Tuning curve" of
individual auditory nerve axon.
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Figure 26: Increasing rate of spike
discharge for auditory nerve axon
with increasing stimulus levels.
Variable is frequency of stimulus
(kHz).
Figure 27: Spike train of auditory
nerve axon, showing "phase
locking"
Time 
Figures 28 and 29: Post Stimulus Time Histograms
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8. Efferent Control of Cochlear Output
Within the auditory system information processing cannot be considered a simple sequential
event. Instead, the functional organization is best characterized by a system of feedback loops
whereby the information that is transmitted through the central nervous system is being
continually modified on the basis of the immediately preceding auditory events, other sensory
inputs, and internal events. It was noted earlier that at the first stage of auditory processing, the
middle ear, the nervous system regulates the amount of mechanical energy impinging on the
cochlea through contractions of the middle ear muscles. This same influence is seen at the level
of the receptor cell output where the terminations of the olivocochlear bundle can markedly
influence the neural events transmitted to the central nervous system.
Although the degree of specificity with which the olivocochlear efferents influence
information processing has not been determined, the effects of gross stimulation on cochlear
output have been investigated. Electrical stimulation of the olivocochlear bundle during sound
presentation markedly reduces the compound eighth nerve potential, and reduces single fiber
responses in the eighth nerve. In the middle frequency range the maximum inhibition of
cochlear output is equivalent to approximately a 25 dB reduction in acoustic stimulus intensity.
The normal biological significance of this feedback loop is not known for certain. The current
opinion is that it may function to enhance the signal-to-noise resolving power of the inner ear,
especially under noisy conditions.
ORGANIZATION OF THE CENTRAL AUDITORY PATHWAYS
The anatomical subdivisions and connections of the mammalian auditory system are both
complex and not fully understood. Many excellent laboratories studying a variety of animals
offer new data each year regarding both the macro- and micro-circuitry of the central auditory
pathways as well as physiologic and behavioral data on the possible functions of various
subcircuits. It will take many more years (or decades) to unravel all of these pathways and
determine their relevance within the human brain. In this limited overview the major pathways
are subdivided into binaural and monaural. This classification should not be considered either
exclusive or exhaustive but is an attempt to define broad classes of functionally related
pathways. It breaks down altogether in the forebrain (thalamus and cerebral cortex) which will
be considered separately. Within each system there are as many descending pathways as
ascending pathways. The descending pathways undoubtedly provide feedback, feedforward, and
gating information, markedly influencing information flow.
Auditory nerve fibers enter the brain stem at the cerebellopontine recess. The fibers pass the
inferior portion of the resiform body and enter the cochlear nucleus. Immediately upon entering
the cochlear nucleus, most, if not all, axons bifurcate. The ascending branch enters the
anteroventral cochlear nucleus, the descending branch projects to the posteroventral and the
dorsal cochlear nuclei.
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The Anteroventral Cochlear Nucleus (AVCN) initiates what is called the binaural brain stem
pathways (Figure 30). Throughout most of this nucleus the cochlear nerve fibers terminate on
the cell bodies of spheroid or globular shaped neurons with large calyceal endings (end bulbs of
Held) that engulf a large portion of the postsynaptic cellular surface. These endings appear
specialized for highly reliable and rapid transmission of nerve impulses from the cochlea. The
major output of AVCN is to the cell groups of the ipsilateral and contralateral superior olivary
complex. Here binaural information first converges. Within the superior olivary complex many
cellular populations have been identified, only a few of which are discussed here.
Medial Superior Olivary Nucleus (MSO). The MSO is a dorsoventrally aligned sheet of
cells with bipolar dendrites. The medially radiating dendrites receive input from the contralateral
AVCN and the lateral dendrites are innervated by fibers from the ipsilateral AVCN. Each of
these inputs is excitatory, primarily low frequencies are represented, and the cells respond best to
a similar frequency presented to each ear. These attributes are consistent with the finding that
cells of the medial superior olivary nucleus differentially respond to binaural time or phase
differences, known to be important for localization of low frequency sounds. The relatively
large size of this nucleus in man may be related to the importance of localizing speech signals.
The primary output of MSO is into the ipsilateral lemniscus, to terminate in the inferior
colliculus.
Medial Nucleus of the Trapezoid Body (MNTB) and Lateral Superior Olivary Nucleus
(LSO). The second major brain stem circuit involved in binaural information processing
involves the AVCN projections to these nuclei. The lateral superior olive receives an ipsilateral
excitatory input from cells in the ventral cochlear nucleus which respond best to high
frequencies. The contralateral input to these cells is disynaptic. High frequency responsive
AVCN cells send heavily myelinated axons across the midline in the trapezoid body to synapse
on large neurons in the MNTB. This rapid conducting pathway then projects to the homolateral
LSO and is inhibitory. Thus, the neurons of the lateral superior olive receive excitatory input
from the ipsilateral ear and inhibitory input from the contralateral ear. Since the spectral content
of high frequency sounds reaching the eardrum varies considerably as a function of the
localization of the sound source, the "push-pull" organization of these projections would seem to
provide amplification of such cues. This is consistent with the fact that the LSO, although small
in man, is large in animals such as bats and some rodents who are specialized for high frequency
sound communication and localization. The major outflow from the LSO neurons is into the
lateral lemniscus bilaterally, to terminate in the inferior colliculus.
Periolivary Nuclei. In the region of the superior olivary nuclei there are a number of smaller
dispersed cell groups which also receive bilateral input from the cochlear nuclei. The precise
nature of the afferentation to these cells is poorly understood in man. At least some of these cells
are the origin of the olivocochlear-bundle and other cells in this region project back to the
cochlear nuclei. Efferent projections from the inferior colliculus to these nuclei are abundant.
Nuclei of the Lateral Lemniscus. As the lateral lemniscus ascends the dorsolateral brain
stem two cell groups are intermingled among the fibers, the dorsal and ventral nuclei of the
lateral lemniscus. Little is known about the function of the lateral lemniscal nuclei.
Inferior Colliculus. The inferior colliculi are the paired elevations forming the caudal half of
the tectal place. Projections from all of the nuclei mentioned above converge on this region. In
addition, direct projections from the contralateral anteroventral cochlear nucleus converge on the
same region of the inferior colliculus that receives olivary input. The two colliculi communicate
with each other through the collicular commissure. Cells in the inferior colliculus respond
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differently to binaural time and intensify differences and lesions of this area disrupt sound
localization on the contralateral side.
In addition to the ascending binaural pathways stressed here, it should be noted that most of
these cell groups receive descending input from the midbrain and possibly from other regions of
the central nervous system (Figure 32).
Figure 30: Binaural auditory
pathways in the brain stem
illustrated for the left cochlear
nucleus. The connections from the
other cochlear nucleus would form a
mirror image. AVCN =
anteroventral cochlear nucleus:
PVCN = postventral cochlear
nucleus; LSO = lateral superior
olive: MSO = medial superior olive,
MNTB = medial nuclear of the
trapezoid body; VLL = ventral
nucleus of the lateral lemniscus;
DLL = dorsal nucleus of the lateral
lemniscus; IC = inferior colliculus;
MG = medial geniculate nucleus.
MONAURAL PATHWAYS OF THE BRAINSTEM
In parallel with the binaural pathways terminating in the inferior colliculus there is a system
of chiefly monaural pathways. Axons from the dorsal cochlear nucleus project into the lateral
lemniscus via the dorsal acoustic stria (of Monakow) to end in the contralateral inferior
colliculus. Collaterals of these fibers (or other axons) also terminate in one of the lateral
lemniscus nuclei. Similar projections are thought to arise from cells of the posteroventral
cochlear nucleus whose axons cross the midline in the intermediate acoustic stria (of Held) and
issue collaterals to the periolivary nuclei. The dorsal cochlear nucleus also receives a variety of
inputs form other auditory nuclei as well as nonauditory centers. For example, the dorsal
cochlear nucleus receives descending input from the inferior colliculus bilaterally, from the
ventral cochlear nucleus, from the cerebellum, from the reticular formation, and probably from
several other midbrain and brainstem regions. Cells in the dorsal cochlear nucleus have complex
coding characteristics.
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FOREBRAIN AUDITORY PATHWAYS (FIGURE 31)
As indicated above, the inferior colliculus appears to be an obligatory synapse in the auditory
pathways. That is, brainstem pathways projecting to the forebrain terminate in the inferior
colliculus as do descending pathways from the forebrain bound for auditory regions of the brain
stem. Thus, consideration of the forebrain auditory system begins with the ascending brachia of
the inferior colliculus, which have their origin in the inferior colliculus and terminate bilaterally
in the medial geniculate body of the thalamus.
The medial geniculate body is a laminated structure, tonotopically organized orthogonally to
the lamina. The geniculate body should not be considered purely auditory. Like other areas of
the thalamus this nucleus probably serves to combine information from the cortex and the
midbrain through the intermediate thalamic nuclei.
From the medial geniculate body the axons extend beneath the pulvinar nucleus, into the
posterior extremity of the internal capsule, under the putamen and then into the cortical
radiations. In man, the primary auditory cortex is on the inner surface of the superior temporal
gyrus (of Heschl) buried deep in the Sylvian fissure (Brodmann's area 41). Topographically
within this area high frequencies appear represented dorsally, with lower frequencies more
ventral. Surrounding the "primary" auditory cortex are a series of "secondary" auditory fields
(e.g. Brodmann's area 22) which may receive direct projections from the medial geniculate body,
but also connect reciprocally with the primary region as well as with the thalamic nuclei. In
addition, there are transcallosal connections linking auditory regions of the two hemispheres, and
connections between the temporal lobe and "auditory" regions in the parietal cortex. As was true
of the brain stem pathways, the forebrain auditory pathways cannot be considered as simply
relaying information to higher level structures. At each level there is a complex and as yet
poorly understood system of feedback loops. This forebrain descending system includes massive
projections from the cortical regions to the ipsilateral medial geniculate body and to both inferior
colliculi (Figure 32).
Figure 31: Connections of the
intermediate brain stem pathway
(solid lines) and monaural brain
stem pathway (dotted line). As in
Figure 30, only projections from
one side are shown. Forebrain
auditory pathways are dashed
(abbreviations as in Figure 30).
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Figure 32: The major descending
auditory pathways for one side of
the brain (abbreviations as in
Figure 30). (Adapted with
permission from Thompson, G.
Seminars in Hearing, Vol.4, pp.8195, Thieme Medical Publishers,
Inc., New York, 1983).
Little is known regarding the cortical circuitry involved in audition in primates, including
man. Basic issues such as "What cortical areas are receiving auditory information and how are
they connected?" are only now beginning to be learned. The questions "How are speech versus
nonspeech sounds gated?" and "How does auditory information gain access to the classical
speech centers?" remain to be answered.
TONOTOPIC ORGANIZATION
An important principle carried through each level of the auditory pathways is the
maintenance of the topography of the receptor surface.
Figure 33: Schematic of the
topographic projection of points on
the cochlea to the anteroventral
cochlear nucleus (AVCN). Each
region of the cochlea is innervated
by many spiral ganglion cells (G)
whose central axons terminate as a
sheet in the cochlear nucleus,
forming an isofrequency lamina.
These isofrequency lamina are
stacked in the order of their
cochlear innervation to form a
tonotopic organization.
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Figure 34: Sagittal section through
the cochlear nucleus of the cat
showing an electrical penetration
through the dorsal cochlear
nucleus (Dc) and posteroventral
cochlear nucleus (Pv). The best
frequency (in kHz) of neurons
encountered at successive points
along the electrode tract are
indicated to the right. Note that
there is a systematic decrease in
best frequencies until the electrode
enters Pv, at which point a new
decreasing sequence begins.
(From Rose, J.E. et al., Bull. Johns
Hopkins Hosp. 104:211-251,
1959).
Figure 35. A: Cutaway drawing
of monkey brain exposes
auditory cortical areas on
supratemporal plane.
Horizontally shaded area
indicates region in which click
stimuli evoke slowwave
potentials in deeply anesthetized
animals. Crosshatched area is
region within which lesions
produce retrograde
degeneration in medical
geniculate. B: Enlarged
drawing corresponding to
crosshatched area in A and
showing patterns of
representation of frequencies
within this region determined by
evoked potential method.
SOUND SOURCE LOCALIZATION
Sound source localization (i.e. directionality) is an important parameter of sound. The
auditory system begins to define the source of sound at the periphery, where head shape and
pinna shape influence intensity and frequency information related to a sound. This information is
transmitted to the CNS along pathways discussed previously, where temporal precision in action
potential encoding maintains frequency- information on arrival times and intensity level at each
ear. Some of the cellular and physiological mechanisms maintaining action potential precision
include: large, secure synapses; fast, glutamatergic receptors; post-synaptic currents that limit the
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window for action potential recruitment. The mechanisms by which binaural information is
processed at the superior olivary complex (SOC) and more centrally are areas of active research.
The role of the lateral superior olive (LSO) in processing of intensity information is well
established. The role of the medial superior olive (MSO) in processing intraural time differences
(ITDs) is subject to active study. The Jeffress model of delay lines is well supported by data
from barn owls. The analogous Laminaris model describes ITD processing in chickens. In
mammals, there is no strong structural evidence for the existence of delay lines. Current
research is investigating the possible role of inhibitory glycinergic input into the MSO as critical
for the processing of ITD information in mammals.
Figure 36. Binaural processing at
the Lateral Superior Olive.
Neuronal responses in the LSO are
sensitive to sound intensity
differences between ipsilateral and
contralateral ears.
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Figures 37. The Jeffress model proposed to account for binaural information processing in the avian auditory
brainstem.
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