5

Auditory System
Ben M. Clopton
Advanced Cochlear Systems
Herbert F. Voigt
Boston University
5.1 Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5-1
5.2 The Peripheral Auditory System . . . . . . . . . . . . . . . . . . . . . . . . 5-1
The External and Middle Ear The Inner Ear
5.3 The Central Auditory System . . . . . . . . . . . . . . . . . . . . . . . . . . . 5-7
Cochlear Nuclei Superior Olivary Complex Nuclei of
the Lateral Lemniscus Inferior Colliculi
Thalamocortical System
5.4 Pathologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5-14
5.5 Further Topics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5-14
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5-14
5.1 Overview
Human hearing arises from airborne waves alternating 50 to 20,000 times a second about the mean
atmospheric pressure. These pressure variations induce vibrations of the tympanic membrane, movement
of the middle-ear ossicles connected to it, and subsequent displacements of the uids and tissues of the
cochlea in the inner ear. Biomechanical processes in the cochlea analyze sounds to frequency-mapped
vibrations along the basilar membrane, and approximately 3,500 inner hair cells modulate transmitter
release and spike generation in 30,000 spiral ganglion cells whose proximal processes make up the auditory
nerve. This neural activity enters the central auditory system and reects sound patterns as temporal and
spatial spike patterns. The nerve branches and synapses extensively in the cochlear nuclei, the rst of the
central auditory nuclei. Subsequent brainstem nuclei pass auditory information to the medial geniculate
and auditory cortex (AC) of the thalamocortical system.
We extract more information from sound than from any other sense. Although primates are described
as visual animals, speech and music carry more of our cultural and societal meaning than sight or other
senses, and we suffer more from deafness than with other sensory losses. Highly effective adaptations of
auditory processing occur in many animals including insects, amphibians, birds, cetaceans, and bats for
prey acquisition, predator avoidance, intraspecies signaling, and other tasks. This chapter surveys current
understanding of the hearing process.
5.2 The Peripheral Auditory System
5.2.1 The External and Middle Ear
and guided to the middle ear by the external auditory meatus, or ear canal. Sounds are ltered due to the
5-1
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As shown in Figure 5.1, ambient sounds are collected by the pinna, the visible portion of the external ear,
5-2 Biomedical Engineering Fundamentals
Pinna
Middle ear
Malleus
Incus
Semicircular
canals
Facial nerve
Auditory
nerve
Cochlea
Eustachian
tube
Stapes
Tympanic
membrane
Exernal
auditory
meatus
Inner ear
FIGURE 5.1 The peripheral auditory system showing the external-ear structures (pinna and external meatus), the
middle ear, and the inner ear. (Courtesy of Virginia Merrill Bloedel Hearing Research Center, Seattle, Washington.)
geometry of the pinna and sound shadowing effects of the head. In species with movable pinnae selective
scanning of the auditory environment is possible for high frequencies [Geisler, 1998; Kinsler et al., 1999].
The bounding interface between the external and middle ear is the tympanic membrane. Pressure
variations across the membrane move three ossicles, the malleus (hammer) connected to the membrane,
the incus (anvil), and the stapes (stirrup) whose footplate is a piston-like structure tting into the oval
window, anopening to the uid-lled cavities of the inner ear. Ligaments and muscles suspend the middle-
ear ossicles so that they move freely. If sound reaches uids of the inner ear directly, 99.9% of the energy is
reected [Wever and Lawrence, 1954], a 30-dB loss due to the mismatch in acoustic impedance between
air and inner-ear uids. Properties of the external meatus, middle-ear cavity, tympanic membrane, and
middle-ear ossicles shape the responsiveness of a species to different frequencies.
The eustachian tube is a bony channel lined with soft tissue extending from the middle ear to the
nasopharynx. In humans it is often closed, except during swallowing, and provides a means by which
pressure is equalized across the tympanic membrane. The function is clearly observed with changes in
altitude or barometric pressure. A second function of the eustachian tube is to aerate the tissues of the
middle ear.
The volume of the air-lled middle-ear cavity inversely determines the stiffness of the tympanic mem-
brane at low frequencies. A reduction of low-frequency impedance for some desert rodents with large
middle-ear cavities [Ravicz and Rosowski, 1997] enhances detection of predators at a distance. On the
other hand, the mass of the middle-ear ossicles dominates impedance at high frequencies and is related to
head mass [Nummela, 1995]. For this reason small mammals generally have good high-frequency hearing,
often extending above 60 kHz. As sound frequency increases, impedances decrease due to eardrum stiff-
ness and increase due to ossicular mass leaving a middle range where sound transmission to the inner ear
is most efcient, limited only by resistive forces [Geisler, 1999], resonances of the cavities, and mechanical
advantages provided by the tympanic membrane, ossicles, and oval window.
Since the ear canal and middle-ear cavities are, or approximate, closed volumes, they support quarter-
wavelength resonances. The human meatus has a broad resonance between 3 and 4 kHz, enhancing sound
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Auditory System 5-3
pressure at the membrane by 12 dB [Weiner and Ross, 1946; von Bksy, 1950]. This will be modied by
obstructing the meatus with headphones or a hearing aid and must be considered in system designs.
The head and external and middle-ear structures impose a transfer function on sound pressure at
the tympanic membrane [Bateau, 1967; Blauert, 1997]. The monaural (single-ear) head-related transfer
function (HRTF) is a function of sound-source azimuth and elevation relative to pressure waveforms
at the tympanic membrane. It is complex, affecting both sound amplitudes and phases over their spec-
trum. Sound localization, highly dependent on binaural hearing, involves a binaural HRTF combining
the left and right monaural HRTFs. Since the structures determining these functions vary, individu-
alized HRTFs combined with head-position sensing are important for computer synthesis of realistic
three-dimensional sound experiences delivered through headphones [Wightman and Kistler, 1989].
For some source locations, even the shadowing effects of the torso produce HRTF cues [Algazi et al.,
2002].
Since the acoustic impedance of the atmospheric source is much less than that of the aqueous medium
of the inner ear, a very inefcient energy transfer would exist without the external and middle ears. The
ossicles form an impedance transformer with a mechanical advantage that passes the acoustic signal at
the tympanic membrane to inner-ear uids with low loss. Essentially air-based sounds of low-pressure
and high-volume velocity are transformed to uid displacements in the inner ear having high-pressure
and low-volume velocity. Two important mechanisms promote this transfer: the area of the tympanic
membrane is about 20 times that of the footplate of the stapes, and the lengths of the malleus and incus
form a lever advantage from the eardrum to oval window of about 1.3 in humans [Wever and Lawrence,
1954; Geisler, 1998]. The hydraulic piston due to the areal ratio contributes about 26 dB to counteract the
impedance mismatch, and the lever mechanism about 2.3 dB. These concepts of middle-ear mechanisms
hold at frequencies below about 2 kHz, but the tympanic membrane does not behave as a piston at
higher frequencies and can support multiple modes of vibration. Second, the mass of the ossicles becomes
signicant contributing to resonances. Third, connections between the ossicles are not lossless, and their
stiffness cannot be ignored. Fourth, pressure variations in the middle-ear cavity can change the stiffness
of the tympanic membrane, as do reexive contractions of middle-ear muscles, especially in response
to intense sounds. Fifth, the cavity of the middle ear produces resonances at acoustic frequencies. All of
these factors produce variations in high-frequency acoustic transmission from the external to the inner
ear specic to individuals, species, and conditions.
5.2.2 The Inner Ear
The acoustic portion of the mammalian inner ear is a spiral structure, the cochlea (snail), containing a
central core, the modiolus, where bers of the auditory nerve collect. The nerve bers arise from spiral
ganglion cells (SGCs) whose somas formthe spiral ganglion in a bony canal around the modiolus. Around
the modiolus spiral three uid-lled chambers or scalae, the scala vestibule (SV), the scala media (SM),
uid in the SV through the oval window. At the other end of the spiral, the apex of the cochlea, the SV
and the ST communicate through the helicotrema. Both are lled with perilymph, similar to extracellular
uid. The SM spirals between them and is lled with endolymph, a medium high in K+ and low in
Na+ due to active processes in the stria vascularis lining the lateral wall. A positive potential of 80 mV is
maintained in the SM by the metabolically driven ionic pumps of the stria vascularis. The SM is separated
from the SV by Reissners membrane, which is impermeable to ions. The SM is separated from the ST by
the basilar membrane (BM) with a length of about 31 mm over 2.5 spiral turns in human [Wever and
Lawrence, 1954]. Resting on the BM is the organ of Corti consisting of one row of inner hair cells (IHCs)
that transduce acoustic signals into neural signals, three rows of outer hair cells (OHCs) that play an
active role in the biomechanics of the cochea, cells that support the hair cells, and the tectorial membrane
overlying the stereocilia of the hair cells.
Stapes displacements for tones above behavioral threshold are very small, estimates of 0.0001 nm
being common [Geisler, 1998]. This can be compared to 0.1 nm for the diameter of a hydrogen atom.
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and the scala tympani (ST) as shown in Figure 5.2. At the base of the cochlea the stapes footplate displaces
5-4 Biomedical Engineering Fundamentals
Reissners
membrane
Stria
vascularis
Organ
of corti
Neurons
FIGURE 5.2 A cross-sectional representation of one turn of the cochlea.
The structures of the inner ear transformthese innitesimal movements to neural discharges that underlie
the detection of sounds.
5.2.2.1 The Basilar Membrane
The cochlear partition (BM and organ of Corti) provides the primary passive mechanical lter function
of the inner ear. Alternating uid displacements at the footplate of the stapes induce pressure differences
across the partition from its base near the oval window to its apex near the helicotrema. The cochlear
partitionhas graded mechanical properties favoring rapid movement to high frequencies near the base and
slower movement to low frequencies near the apex resulting in a traveling wave motion in that order. The
membranes width varies as it traverses the cochlear duct, narrower at its basal end than at its apical end.
It is stiffer at the base than at the apex, with stiffness varying by about two orders of magnitude. Pressure
relief is provided for the incompressible uids of the inner ear by the round window, a membrane-covered
opening from the ST to the middle-ear cavity. A transient pressure increase (condensation) at the stapes
displaces its footplate inward, a traveling wave is initiated along the BM, pressure is increased in the ST,
and a compensatory outward displacement of the round window membrane occurs. A rarefaction causes
the round window membrane to move inward toward the ST.
Sound decomposition into its frequency components is a major function of the cochlea. Georg von
Bksy observed the traveling wave on the cochlear partitions of cadavers under stroboscopic light syn-
chronized to high-intensity, low-frequency tones. The traveling wave reached a maximum displacement
along the BM depending on the frequency of the tone indicating a roughly logarithmic mapping of
increasing frequencies from the apex to the base. His experiments on the peripheral auditory system are
collected in a book [von Bksy, 1950], and he was awarded the 1961 Nobel Prize in medicine for his
research.
Movements of the BM are very small, in the nanometer range or less for normal hearing, and a new
technique increased measurement resolution to this level [Johnstone and Boyle, 1967]. The Mssbauer
technique uses Doppler shift in emissions from a small radioactive particle placed on the moving tissue
being observed. In 1971, Rhode published Mssbauer measurements of tuning in the basal region of the
living cochlea. These tuning curves were remarkably sharp (Q
10
of 7 to 8) for pure tones at low intensities,
but they degraded to broad tuning at high intensities. The slopes of the tuning curve are much greater at
the high-frequency edge than at the low-frequency edge. In the absence of an explanation using passive
models, these and subsequent observations came to implicate active tuning processes in the cochlea,
sometimes called the cochlear amplier.
Measurements using laser interferometer techniques now allow displacement resolutions of less than a
nanometer [Mammano and Ashmore, 1995] and have aided investigations of the cochleas active tuning
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Auditory System 5-5
FIGURE 5.3 A depiction of the organ of Corti and its cellular structures. TM: tectorial membrane elevated to show
stereocilia, PC: inner and outer pillar cells, DC: Deiters cells, RL: reticular lamina, SC (IHC): one row of stereocilia
for IHCs, SC (OHC): three rows of stereocilia for OHCs, HC: Hensens cells. Other abbreviations are as used in text.
Synapses from SGCs are seen at the bottoms of IHCs with efferent axons to OHCs seen in the tunnel and passing
between Deiters cells.
mechanisms. It has been discovered that the cochlear amplier operates primarily in the basal, high-
frequency regions and is highly compressive, that is, large increases in high-frequency tone intensity cause
small increases in the maximum displacement of the BM [Geisler, 1998].
5.2.2.2 The Organ of Corti
As shown in Figure 5.3, the organ of Corti is comprised of supporting cells, the hair cells themselves, and
the tectorial membrane. The ciliated ends of both OHCs and IHCs are rigidly xed by supporting cells,
for example, Deiters cells form the reticular lamina, a rigid plate holding the upper ends of the OHCs.
Pillar cells form a rigid triangular tunnel whose upper surface extends the reticular lamina. The reticular
lamina and upper ends of the pillar cells and other support cells form a barrier to ions, thereby isolating
the endolymph of the SM from the perilymph of the ST surrounding the lower parts of the hair cells.
Both IHCs and OHCs have precise patterns of stereocilia at the end held within the rigid plate formed
by supporting cells. The tectorial membrane overlies the stereocilia, but while those of OHCs contact the
tectorial membrane, the stereocilia of the IHCs do not. At the end opposite the stereocilia, IHCs synapse
with the distal processes of SGCs. The proximal processes of SGCs are generally myelinated and form
most of the auditory nerve. The nerve is laid down as these bers collect from the apex and base in an
orderly spiral manner. The nerve retains the frequency map of the BM, that is, it is tonotopically organized,
a characteristic that carries through much of the auditory system.
5.2.2.2.1 Inner Hair Cells
The IHCs lie in a single row on the modiolar side of the organ of Corti and number between 3000 and
4000 in human [Nadol, 1988]. The IHCs stereocilia are of graded, increasing length from the modiolar
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TM
SC (IHC)
SC (OHC)
RL
HC
DC
OHC
BM
PC
IHC
20 mm
5-6 Biomedical Engineering Fundamentals
side of the cell. Early in ontogeny, a kinocilium is positioned next to the longest stereocilia, and excitation
of hair cells occurs from ciliary displacement in that direction further opening membrane channels to
potassium and depolarizing the cell [Hudspeth, 1987]. The positive potential in the endolymph of the SM
drives K+ ions through the gating mechanism of IHC stereocilia to the negative intracellular potential.
Displacement in the other direction reduces channel opening and produces a relative hyperpolarization
[HudspethandCorey, 1977]. These changes inintracellular potential modulate transmitter release through
vesicle exocytosis at the base of the IHCs. The transmitter is related to glutamate but not glutamate itself
[Gleich et al., 1990].
The IHCs are not attached to the tectorial membrane, so their response is thought to be responsive
to uid velocity over their stereocilia rather than direct displacement. Hair cells in some species exhibit
frequency tuning when isolated [Crawford and Fettiplace, 1985], but mammalian hair cells do not. The
tuning of the mammalian auditory system arises from the motions of the cochlear partition, and this is
transferred to the IHCs and to the rest of the auditory system through their connection to SGCs. The
nature of membrane channels and molecular mechanisms in auditory hair cells is being examined using
a number of techniques [Hudspeth, 2000; Ashmore and Mammano, 2001].
5.2.2.2.2 Outer Hair Cells
There are about 12,000 OHCs in the human cochlea [Nadol, 1988]. They have primarily efferent innerv-
ation, a puzzling arrangement for many years since the cochlea was a sensory organ. The discovery
of cochlear tuning that was not readily explainable from passive mechanical properties shifted atten-
tion to the OHCs where research, over the last few decades, has focused on their cellular and molecular
mechanisms.
It was discovered that electrical stimulation of isolated OHCs produced lengthening or shortening
[Brownell et al., 1985]. It is generally accepted that the motility of OHCs counters viscous drag from
uids and cells of the cochlear partition. Through their contact to the tectorial membrane they sense
the subnanometer displacements of the BM and feedback, in phase, to augment them. This positive
feedback occurs at auditory frequencies and is responsible for cochlear amplication. It occurs, or is most
obvious, at low sound intensities, so it is responsible for the incredible sensitivity of the ear and for the
nonlinear compression of the dynamic range of intensity coding. It was also observed that iontophoretic
application of acetylcholine to the synaptic end of OHCs causes them to shorten. Efferents to OHCs
release acetylcholine and thereby modulate the mechanical properties of the cochlea. The OHCs appear to
affect the response of the auditory system in several ways. They enhance the tuning characteristics of the
system to sinusoidal stimuli, decreasing thresholds and narrowing the lters bandwidth, and they likely
inuence the damping of the BM dynamically by actively changing its stiffness.
Before the role of OHCs was determined it was observed that sounds could be measured in the
meatus, both spontaneously and in response to other sounds [Wilson, 1986]. In humans they tend
to contain spectrally narrow components and vary across individuals. OHCs are strongly implicated
as the source for these emissions because sounds in the opposite ear affect them (presumably through
the efferent system) and aspirin, known to affect OHCs, reduces them [Geisler, 1998]. As with most
positive-feedback systems, spontaneous oscillation is suggested. Otoacoustic emissions are becom-
ing important in the clinical evaluation of cochlear function for their potential signaling of cochlear
pathologies.
5.2.2.3 Spiral Ganglion Cells and the Auditory Nerve
The auditory nerve of the human contains about 30,000 afferent bers. Most (93%) are heavily myelinated
and arise fromType I SGCs whose distal processes synapse on IHCs. The rest are fromsmaller, more lightly
myelinated Type II SGCs. Each IHC has, on average, a number of Type I SCCs that synapse with it, 8 in
the human and 18 in the cat. In contrast, each Type II SGC contacts OHCs at a rate of about 10 to 60 cells
per ber. The tonotopically organized nerve (low-frequency bers in the center and high-frequency bers
in the outer layers) exits the modiolus and enters the internal auditory meatus of the temporal bone on
its path to the cochlear nuclei.
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Auditory System 5-7
Discharge spike patterns from the nerve have typically been characterized with repeated tone bursts
varied in frequency and intensity [Kiang, 1965]. Three views of the data are commonly used:
1. The temporal pattern of response to a tone burst is summarized in a peristimulus time histogram
(PSTH). Auditory neurons may discharge only a few times during a brief tone burst, but if a
histogram of spike events is synchronized to the onset of repeated tone bursts, a PSTH results that
is more statistically representative of the neurons response. Discharge patterns fromthe nerve have
2. Arate-level function of spike counts vs. intensity at one tonal frequency has a threshold level, where
counts rise from quiet levels, and a maximum rate, often a plateau holding for further increases
in intensity. The range from threshold to the maximum, or saturation, level is called the dynamic
range for sound-intensity signaling by response rate changes. A spontaneous rate of discharge,
ranging from 50 spikes per second to less than 10, is usually measured for subthreshold stimulus
levels.
3. Fiber responses are also characterized with tuning curves, a plot of thresholds for stimulus intensity
vs. frequency. Tuning curves for auditory nerve bers have a minimum intensity (maximum
sensitivity) at a characteristic frequency (CF).
Sounds are coded in nerve discharges in two major ways: the level of discharge activity within the ber
population reects the spectrum of sounds (labeled-line or place coding), and the temporal pattern
of discharges in a ber is partially synchronized to the cycle-by-cycle timing of frequencies near its
CF (temporal synchrony coding). Furthermore, complex sounds undergo nonlinear interactions in the
cochlea, an example being two-tone suppression where the introduction of a new tone reduces both the
discharge rate and synchrony of a ber to CF tones [Geisler, 1998].
While these coding mechanisms were discovered with tones, Sachs and Young [1979] found that
the spectra of lower-intensity vowel sounds are represented as corresponding tonotopic rate peaks in nerve
activity, but for higher intensities this place code is lost as discharge rates saturate. At high intensities, spike
synchrony to frequencies near CF continue to signal the relative spectral content of vowels, a temporal
code. These results hold for high-spontaneous-rate bers (over 15 spikes sec), which are numerous.
Less common, low-spontaneous-rate bers (<15 spikes sec) appear to maintain the rate code at higher
intensities, suggesting different coding roles for these two ber populations. Furthermore, it has more
recently been argued that these results from the cat do not represent the human cochlea. When vowels are
spectrally scaled to match the cats cochlea, the rate code appears to remain at high intensities [Recio et
al., 2002].
5.3 The Central Auditory System
The central auditory system consists of the cochlear nuclei; groups of brainstem nuclei including the
superior olivary complex (SOC) , nuclei of the lateral lemniscus (LL), and inferior colliculus (IC); and the
auditory thalamocortical system consisting of the medial geniculate in the thalamus and multiple areas of
are not shown. Page constraints prevent us from providing uniform detail for all levels of the auditory
system.
5.3.1 Cochlear Nuclei
Many studies have focused on the anatomy and physiology of the cochlear nucleus (CN) revealing a
wealth of information. It can be subdivided into three regions, the anteroventral CN (AVCN) anterior
to the nerve entry, the posteroventral CN (PVCN), and the dorsal CN (DCN), each with one or more
distinctive neuron types and connections. The axon from each Type I SGC in the nerve branches to each
of the three divisions in an orderly manner so that tonotopic organization is maintained. Neurons with
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a primary-like pattern (see Figure 5.5).
the cerebral cortex. Figure 5.4 schematically indicates the nuclear levels and pathways. Efferent pathways
5-8 Biomedical Engineering Fundamentals
MGB
AC
IC
NLL
DCN
VCN
SOC
FIGURE 5.4 Schematic of the auditory system. Some of the major pathways and connections have been represented.
The system is bilaterally symmetrical (midline as dashed line), paths are crossed and shown for one side in most cases
for clarity.
to receive connections from Type II SGCs.
Morphologic categories based on shapes of dendritic trees and somas include spherical bushy cells in
the anterior part of the AVCN, both globular bushy cells and spherical bushy in posterior AVCN, stellate
cells throughout the AVCN and in the lower layers of the DCN, octopus cells (asymmetrical dendritic tree
resembling an octopus) in the PVCN, and fusiform and giant cells in DCN. In AVCN spherical bushy cells
receive input fromone Type I ganglioncell througha large synapse formationcontaining endbulbs of Held,
while the globular cells receive inputs froma fewafferent bers. The AVCNis tonotopically organized, and
repeated with variation through most auditory nuclei. The DCN is structurally the most intricate of the
CN subnuclei having four or ve layers in many species giving it a cortical structure comparable to
simultaneous recording from pairs of physiologically identied DCN units and responses to tones and
noise has allowed the development of conceptual models of DCN neuronal circuitry in cat [Young and
Brownell, 1976; Voigt and Young, 1980, 1990; Young and Davis, 2002] and gerbil [Davis and Voigt, 1997].
Although some differences between the two species have been noted, these may well be explained by a
similar underlying neural circuit model whose parameters are somewhat species specic (as opposed to
completely different neuronal architectures) [Davis and Voigt, 1997].
Intracellular recording in slice preparation has identied the membrane characteristics of CN neuronal
types [Bal and Oertel, 2001; Manis, 1990]. Some of these characteristics have been conrmed in vivo
[Hancock and Voigt, 2002]. The diversity of neuronal morphologic types, their participation in local
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neurons having similar CFs formlayers calledisofrequency laminae[Bourk et al., 1981], an organization
the cerebellum [see Young, 1998; Oertel and Young, 2004]. Extracellular recording techniques, including
common morphologic classications are found in all three divisions, especially granule cells, which tend
Auditory System 5-9
Primary-Like (PL)
Chopper (C)
S
p
i
k
e
s
/
s
e
c
o
n
d
Primary with notch
(PLn)
Pauser (P) Buildup (B)
Onset (O)
Stimulus
0 100
Time (msec)
FIGURE 5.5 PSTH categories obtained for neural spike activity in the nerve and cochlear nuclei in response to brief
tone bursts (stimulus envelope shown in lower left). Discharges in the nerve have the PL pattern while the others are
associated with regions of the VCN and DCN and with specic morphological types.
circuits, and the emerging knowledge of their membrane biophysics are motivating detailed modeling
[Babalian et al., 2003].
5.3.1.1 Spike Discharge Patterns
Tone bursts at a cells CF and 40 dB above threshold produce PSTHs with shapes distinctive to different
nuclear subdivisions and even different morphologic types. PSTH patterns provide insight into sound
features exciting auditory neurons. Figure 5.5 illustrates the major PSTH pattern types obtained from
the auditory nerve and CN. Auditory nerve bers and spherical bushy cells in AVCN have primary-like
patterns in their PSTHs, an elevated spike rate after tone onset, falling to a slowly adapting level until the
tone burst ends. Globular bushy cells may have primary-like, pri-notch (primary-like with a brief notch
after onset), or chopper patterns. Stellate cells have nonprimary-like patterns. Onset response patterns,
one or a few brief peaks of discharge at onset with little or no discharges afterward, are observed in
the PVCN from octopus cells. Chopper, pauser, and buildup patterns are observed in many cells of the
DCN. For most CN neurons, these patterns are not necessarily stable over different stimulus intensities;
a primary-like pattern may change to a pauser pattern and then to a chopper pattern as intensity is raised
[Young, 1984].
Because central neurons often have inhibitory inputs, some stimuli reduce discharge probabilities, and
patterns, but many variations have been observed on these. Fibers and neurons with primary-like PSTHs
generally have response maps with only an excitatory region (Figure 5.6a) although controls must be
used to identify two-tone suppression. The lower edges of this region approximate the threshold-tuning
curve. Octopus cells often have very broad tuning curves and extended response maps, as suggested by
their frequency-spanning dendritic trees. More complex response maps are observed for some neurons,
such as those in the DCN. Inhibitory regions alone, a frequencyintensity area of suppressed spontaneous
discharge rates, or combinations of excitatory and inhibitory regions have been observed. Some neurons
are excited only within islands of frequencyintensity combinations, demonstrating a CF but having
no response to high-intensity or wide-band sounds [Spirou et al., 1999]. Response maps in the DCN
containing both excitatory and inhibitory regions have been shown to arise from a convergence of inputs
from neurons with only excitatory or inhibitory regions in their maps [Young and Voigt, 1981].
Categorization of CN neurons increasingly depends on many measures: cellular morphology, PSTH
and response-eld response patterns tones, responses to wide-band stimuli and binaural stimuli,
membrane channel physiology, afferent and efferent connectivity, and molecular expressions and
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so threshold tuning curves are extended to response-eld maps. Figure 5.6 shows three response-eld
5-10 Biomedical Engineering Fundamentals
FIGURE 5.6 Response-eld maps characteristic of auditory-nerve bers (a) and central neurons. Two-tone suppres-
sion in the cochlea, not due to inhibitory synapses, may resemble panel b maps. Maps are extracted from discharge
rates sampled over the stimulus intensityfrequency parameter space. The inhibitory areas represent decreases in
spontaneous or evoked discharge rates by tone bursts of the frequency and intensity under test.
responses [Spirou et al., 1999; Fujino and Oertel, 2001]. Beyond mere cellular categorization, information
processing in the CN is being discovered as the functions of neuronal circuits are dissected.
Principal neurons of cats [Spirou and Young, 1991] and gerbils [Parsons et al., 2001] have shown to
be sensitive to spectral notches like those appearing in HRTFs. These notches, whose center frequency
changes with elevation, are thought to be cues for sounds localized in the median plane, where interaural
time and intensity cues are absent. Thus, part of the function of the DCN may be to aide in median plane
sound localization. The DCN, however, integrates these spectral cues with information from the somato-
sensory and vestibular systems, as well as from descending auditory pathways. The DCN shows signs of
both long-term potentiation (LTP) and long-term depression (LTD) of some of its synapses, providing
exclusively during development (e.g., when we need to learn to associate specic spectral notch frequen-
cies with specic median plane locations) or if they function in adults navigating within their acoustic
environments remains a topic of intense interest.
In addition to the contributions to our understanding of CN function gained through anatomy,
physiology, pharmacology, and behavioral approaches, computational modeling of the neuronal cir-
cuitry of the CN has also contributed to our understanding of CN function. Auditory nerve models have
provided the front ends to CN models [Carney, 1993]. Single CN neurons [Kim et al., 1994, Hewitt and
Meddis, 1995] as well as neural populations have been modeled [Voigt and Davis, 1996; Hancock and
Voigt, 1999]. Amajor reason for computational modeling of the neuronal circuitry is to verify the behavior
of the model, compare it to the known physiology, and to predict behavior of the model to novel stimuli
2006 by Taylor & Francis Group, LLC
[see Hancock et al., 1997; Nelkin et al., 1997].
Excitatory
(a)
(b)
(c)
Inhibitory
Frequency
S
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n
s
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CF
the infrastructure for learning [see Oertel andYoung, 2004]. Whether these learning mechanisms are used
Auditory System 5-11
5.3.2 Superior Olivary Complex
The SOC contains ten or more subdivisions in some species. It is the rst major site at which connec-
tions from the two ears converge and is therefore a center for binaural processing that underlies sound
localization. There are large differences in the subdivisions between mammalian groups such as bats,
primates, cetaceans, and burrowing rodents that utilize vastly different binaural cues. Binaural cues to
the locus of sounds include interaural level differences (ILDs), interaural time differences (ITDs), and
detailed spectral differences for multispectral sounds due to head and pinna ltering characteristics. These
are summarized in the binaural HRTF [Tollin and Yin, 2001].
The medial superior olive (MSO) and lateral superior olive (LSO) process ITDs and ILDs, respectively.
Aneuron in the MSOreceives projections fromspherical bushy cells of the CNfromboth sides and thereby
the precise timing and tuning cues of nerve bers passed through the large synapses mentioned. The tem-
poral accuracy of the pathways and the comparison precision of MSO neurons permit the discrimination
of changes in ITD of a few tens of microseconds. MSO neurons project to the ipsilateral IC through the
LL. Globular bushy cells of the CN project to the medial nucleus of the trapezoid body (MNTB) on the
contralateral side, where they synapse on one and only one neuron in a large, excitatory synapse, the calyx
of Held. MNTB neurons send inhibitory projections to neurons of the LSO on the same side, which
also receives excitatory input from spherical bushy cells and probably other neurons in the AVCN on the
same side [Doucet and Ryugo, 2003]. Sounds reaching the ipsilateral side will excite discharges from an
LSO neuron, while those reaching the contralateral side will inhibit its discharge. The relative balance of
excitation and inhibition is a function of ILD resulting in this cue being encoded in LSO discharge rates.
One of the subdivisions of the SOC, the dorsomedial periolivary nucleus (DMPO), is a source of efferent
bers that reach the contralateral cochlea in the crossed olivocochlear bundle (COCB). Neurons of the
DMPO receive inputs from collaterals of globular bushy cell axons of the contralateral ACVN that project
to the MNTB and from octopus cells on both sides. The functional role of the feedback from the DMPO
to the cochlea is not well understood.
5.3.3 Nuclei of the Lateral Lemniscus
The LL consists of ascending axons from the CN and LSO. The nuclei of the lateral lemniscus (NLL)
lie within this tract, and some, such as the dorsal nucleus LL (DNLL), are known to process binaural
information [Burger and Pollak, 2001], but less is known about these nuclei as a group than others,
partially due to their relative inaccessibility.
5.3.4 Inferior Colliculi
The IC are paired structures lying on the surface of the upper brainstem. Each colliculus has a large
central nucleus, the ICC, a surface cortex, and paracentral nuclei. Each colliculus receives afferents from a
number of lower brainstem nuclei, projects to the medial geniculate body (MGB) through the brachium,
and communicates with the other colliculus through a commissure. The ICCis the major division and has
distinctive isofrequency laminae formed from cells with disk-shaped dendritic trees and afferent bers.
The terminal endings of afferents form brous layers between laminae. The remaining neurons in the
ICC are stellate cells that have dendritic trees spanning laminae. Axons from these two cell types make up
much of the ascending ICC output.
Both monaural and binaural information converge at the IC through direct projections from the CN
and from the SOC and NLL. Crossed CN inputs and those from the ipsilateral MSO are excitatory.
Inhibitory synapses in the ICC arise from the DNLL, mediated by gamma-amino-butyric acid (GABA),
and from the ipsilateral LSO, mediated by glycine [Faingold et al., 1991].
These connections provide an extensive base for identifying sound direction at this midbrain level,
but due to their convergence, it is difcult to determine what binaural processing occurs at the IC as
opposed to being passed from the SOC and NLL. Many neurons in the IC respond differently depending
on binaural parameters. Varying ILDs for clicks or high-frequency tones often indicate that contralateral
2006 by Taylor & Francis Group, LLC
5-12 Biomedical Engineering Fundamentals
sound is excitatory. Ipsilateral sound may have no effect on responses to contralateral sound, classifying
the cell as E0, or it may inhibit responses, in which case the neuron is classied as EI, or maximal excitation
may occur for sound at both ears, classifying the neuron as EE. Neurons responding to lower frequencies
are inuenced by ITDs, specically the phase difference between sinusoids at the ears. Spatial receptive
elds for sounds are not well documented in the mammalian IC, but barn owls, who use the sounds of
prey for hunting at night, have sound-based spatial maps in the homologous structure [Knudsen and
Knudsen, 1983; Bala et al., 2003]. In mammals and owls the superior colliculus, situated just rostral to the
IC and largely visual in function, has spatial auditory receptive eld maps.
5.3.5 Thalamocortical System
5.3.5.1 Medial Geniculate
The MGB and AC form the auditory thalamocortical system. As with other sensory systems, extensive
projections to and from the cortical region exist in this system. The MGB has three divisions, the ventral,
dorsal, and medial. The ventral division is the largest and has the most precise tonotopic organization.
Almost all its input is from the ipsilateral ICC through the brachium of the IC. Its large bushy cells have
dendrites oriented so as to lie in isofrequency layers, and the axons of these neurons project to the AC.
5.3.5.2 Auditory Cortex
As suggested previously, it is inaccurate to view central auditory pathways as a frequency-mapped sensory
conduit to higher centers. The auditory system, indeed the entire brain operates to ensure survival by
promoting effective behaviors and storing experience in memory for future decisions. In essence, audition
identies critical sound events and associates them with appropriate responses. This is evident in many
observations at the cerebral cortex, but examples for bats and human speech suggest the range and
complexity of processing in auditory pathways.
5.3.5.2.1 Bat Cortex
Bats of the suborder Microchiroptera use echos from cries they emit to locate and capture prey, usually
insects. A well-studied species, the mustached bat (Pteronotus parnellii) emits brief sounds with a fun-
damental continuous frequency (CF) around 30 kHz with a short downward frequency-modulated (FM)
sweep at the end. This cry has strong harmonics, so much of the returning energy is at multiples of the
fundamental. This CFFM sound is just one strategy used by various Microchiroptera, but the role of the
cortex. In an expanded region of a tonotopic map is the Doppler-shifted CF (DSCF) area with responses
to the second harmonic of the 30-kHz chirp the bat emits. Cochlear specializations in this bats inner
ear greatly emphasize frequency resolution in the 60-kHz region. Specically, returning CF sounds are
mapped so precisely that the Doppler shift produced by insect wing utters will cause the site of maximum
activity to vary. Another area, the CF/CF area, compares the frequency of the returning CF signal with
that of the emitted signal, a cue for the relative velocity of the prey. The FMFM region responds to the
time difference between the emitted and returning FM cry components as a cue to the distance of the prey
[Suga, 1990].
To illustrate the variation in cortical function, it is noted that other species of bats process sound
differently in their auditory cortices. The pallid bat uses echolocation for obstacle avoidance and passive
listening to locate prey [Razak and Fuzessery, 2002]. As with the mustached bat, echolocation uses
frequencies above 30 kHz, but prey location uses frequencies below 20 kHz, and neuron responses differ
accordingly over the tonotopic map at cortex.
5.3.5.2.2 Human Cortex
The understanding and production of speech has evolved in human-ancestral primates over the last two
hundred thousand years and are mediated by the primary AC and surrounding areas. The primary AC
is tonotopically organized, but surrounding areas implicated in higher-level language functions are not
2006 by Taylor & Francis Group, LLC
AC in the mustached bat has been extensively studied. Figure 5.7 shows responsive regions in this bats
Auditory System 5-13
Delay
axis
2 mm
Azimuthal
axis
DSCF area
FIGURE 5.7 Auditory cortical areas of the mustached bat showing selective processing in different cortical areas for
the emitted and returning components of the CF-FM echolocation cry. (Adapted from Suga [1990]. Sci. Am. 262:
6068.)
Brocas area
Precentral gyrus
Central sulcus
Postcentral
gyrus
Wernickes area
Auditory
FIGURE 5.8 Cortical areas in human involved with hearing and language. The auditory areas are located on the
temporal lobe, the primary area (A1) being on the dorsal surface within the Sylvan sulcus (not visible). Broca and
Wernickes areas are involved with the production and understanding of language.
easily analyzed. Studies of stroke and injury have helped differentiate the roles of these areas. In most
individuals these functions are limited to the left side of the brain.
Figure 5.8 shows the major regions of auditory and language processing relative to common cortical
landmarks. The primary auditory area is on the upper surface of the temporal lobe (not shown), but
supplementary areas are located on the lateral temporal lobe. Brocas area is located in the posterior
portion of the frontal lobe near the auditory regions in the temporal lobe. Wernickes area is in the
2006 by Taylor & Francis Group, LLC
5-14 Biomedical Engineering Fundamentals
posterior part of the temporal lobe. Regions surrounding these also participate in language, but it is
difcult to dene many of the functions involved because they involve mixtures of speech production and
understanding with subtle grammatical and logical relationships.
Two clinical conditions arising from stroke or injury have been studied extensively, Brocas and Wer-
nickes aphasias. Damage to Brocas area will often lead to labored but generally correct speech production,
but spoken sentences with complex grammars will not be understood. The concept that Brocas area
provides short-term working memory for the comparison of sentence components has been suggested. In
contrast, patients with damage to Wernickes area will often speak effortlessly but with many lexical errors,
and they generally do not understand sentences spoken by others. Wernickes area, once thought to under-
lie speech comprehension is now considered a link between areas for concept and meaning with those
for word choice and grammar. Wernickes area is often grouped with the supramarginal gyrus (SMG)
just above it. A third clinical syndrome, conduction aphasia, results from damage to neural pathways
linking Wernickes to the SMG and Brocas area. Speech production and understanding is less affected in
conduction aphasia, but it has distinctive features including an inability to repeat sentences accurately and
difculty in naming things.
Signicant variations arise over the range of clinical damage to cortical and white matter surrounding
these areas, especially the SMG, and if tissue damage is restricted to a small area, the aphasia may be
transient. Auditory input at the cortical level goes far beyond tonotopic organization to complexities of
language, and when it is absent other sensory input may take over. An example of the generality of function
is the disruption of signing by a deaf patient during electrical stimulation of these areas during awake brain
surgery for temporal lobe epilepsy [Corina et al., 1999]. Tissues normally involved with understanding
and producing speech switch to visual cues with deafness.
5.4 Pathologies
Hearing loss results from conductive and neural decits. Conductive hearing loss due to attenuation in
the outer or middle ear often can be alleviated by amplication provided by hearing aids and may be
subject to surgical correction. Sensorineural loss due to the absence of IHCs results from genetic decits,
biochemical insult, and exposure to intense sound, or aging (presbycusis). For some cases of sensorineural
loss, partial hearing function can be restored with the cochlear prosthesis, direct electrical stimulation of
remaining SGCs using small arrays of electrodes inserted into the ST (see chapter on cochlear implants)
As of 2004, an estimated 70,000 people have received cochlear implants.
Lesions of the nerve and central structures occur due to trauma, tumor growth, and vascular accidents.
These may be subject to surgical intervention to prevent further damage and promote functional recovery.
In patients having no auditory nerve due to tumor removal, direct electrical stimulation of the CN has
been used to provide auditory sensation.
5.5 Further Topics
In a brief survey it is not possible to cover many important topics for the auditory system. Excellent
books treat these in detail. A great deal of attention has been and is being paid to plasticity in neural
and behavioral mechanisms of hearing [Parks et al., 2004]. Likewise, little has been said about perceptual
mechanisms and the techniques for assessing the behavioral limits of hearing [Hartmann, 1998].
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