373 7

The Auditory System

Hans J. ten Donkelaar and Kimitaka Kaga

Brödel’s drawing of the ear

Contents

7.1 Introduction – 375

7.2 The Cochlea and the Cochlear Nerve – 376
7.2.1 T he Middle Ear and the Cochlea: Mechanical Transmission
of Sound – 376
7.2.2 Cochlear Hair Cells: Transduction and Amplification – 378
7.2.3 Spiral Ganglion Cells and the Cochlear Nerve:
Neural Transmission – 378
7.2.4 The Auditory Periphery: Generation of Evoked Activity – 380
7.2.5 Hearing Loss – 380

© Springer Nature Switzerland AG 2020

H. J. ten Donkelaar, Clinical Neuroanatomy, https://doi.org/10.1007/978-3-030-41878-6_7
7.3 The Brain Stem Auditory System – 385
7.3.1 T he Cochlear Nuclei: Diversification of Cochlear Input – 385
7.3.2 The Superior Olivary Complex: Recreation of Auditory Space – 387
7.3.3 The Upper Brain Stem: Integration of Ascending
Auditory Pathway – 388
7.3.4 Brain Stem Topography: Generation of Evoked Potentials – 389

7.4 The Forebrain Auditory System – 389

7.4.1 T he Auditory Thalamus – 389
7.4.2 The Acoustic Radiation – 389
7.4.3 The Auditory Cortex: Sequential Levels of Auditory Processing – 389
7.4.4 Auditory Disorders Related to Stroke – 395

7.5 The Descending Auditory System – 402

References – 403
7.1 · Introduction
375 7
7.1 Introduction organized. For the terminology, the English terms of the
Terminologia Neuroanatomica (TNA 2017; see ten
The ear or vestibulocochlear organ is composed of Donkelaar et al. 2017, 2018) are used.
external, middle and internal or inner parts (. Fig. 7.1). At birth, humans have about 20,000 inner and outer
The external ear consists of the auricle and the external hair cells in the organ of Corti, which often do not last
acoustic meatus with the outer layer of the tympanic a lifetime as they do not regenerate when lost (Stone
membrane. The middle ear is formed by the tympanic et al. 1998). By the age of 65–75 years, many individuals
cavity, the auditory ossicles and the inner layer of the have a bilateral, high-frequency progressive hearing loss
tympanic membrane. The internal or inner ear com- known as presbycusis associated with hair cell attrition.
prises the labyrinth, a series of fluid-filled spaces in the Hair cell loss is the most common cochlear defect caus-
petrous part of the temporal bone. The auditory part of ing hearing impairment in presbycusis and noise-­
the inner ear consists of the cochlea with the spiral induced hearing loss. The cochlear nerve may be
organ of Corti, which contains hair cells as auditory involved in various types of disorders (see 7 Clinical
receptors. Receptors sensitive to high frequencies are Cases 7.1, 7.2, and 7.3). Hearing disorders due to brain
located near the cochlear base and those sensitive to low stem lesions are rare because of the bilateral projections
frequencies near the apex of the cochlea. The hair cells of the central auditory pathways. Midline lesions of the
are innervated by the peripheral processes of bipolar retropontine tegmentum may result in impaired sound
ganglion cells in the spiral ganglion. Their central pro- localization due to interruption of the input of the
cesses form the cochlear division of the vestibuloco- superior olivary complex (see 7 Sect. 7.3.2 and
chlear nerve and terminate in the cochlear nuclei. The 7 Clinical Case 7.4). Disorders of auditory perception
principal auditory pathway passes from the cochlea, via may follow strokes in the territory of the internal carotid
the cochlear nuclei, the inferior colliculus and the medial arteries or of the vertebrobasilar system. The central
geniculate body (MGB), to the contralateral auditory disorders of auditory perception may result from lesions
cortex on the dorsal surface of the superior temporal of either the right, the left or both cerebral hemispheres,
gyrus. Each MGB is bilaterally innervated, so that each usually involving parietotemporal cortical areas as illus-
hemisphere receives cochlear input bilaterally. All of the trated in 7 Clinical Cases 7.5, 7.6, 7.7, 7.8, and 7.9 (see
components of the auditory pathway are tonotopically 7 Sect. 7.4.4).

..      Fig. 7.1 Overview of the

external, middle and internal ear.
(From Brödel 1946)
 376 Chapter 7 · The Auditory System

7.2 The Cochlea and the Cochlear Nerve trigeminal nuclei, respectively (Lyon 1978; Mizuno
et al. 1982; Shaw and Baker 1983). The stapedius mus-
7.2.1  he Middle Ear and the Cochlea:
T cle functions to protect the auditory receptors of the
Mechanical Transmission of Sound inner ear against excessive stimulation caused by too
strong sound pressure. The sound pressure depends on
the amplitude of the waves: the greater the amplitude,
The middle ear comprises the tympanic cavity, the tym-
the higher the sound pressure. The stapedius muscle
panic membrane, the three auditory ossicles, two middle
contracts in response to sounds above 70 dB (the inten-
ear muscles, air-filled cavities formed by the mastoid
sity of loud conversation), damping the movements of
antrum and mastoid air cells and the auditory tube. The
the auditory ossicle chain. The tensor tympani muscle
tympanic cavity communicates with these air-filled cavi-
contracts to louder sounds, especially impulse noises.
ties and through the auditory tube with the nasopharynx
The acoustic middle ear reflex includes projections from
(. Fig. 7.1). The three auditory ossicles are the hammer
the ventral cochlear nucleus via the superior olivary
or malleus, the anvil or incus and the stirrup or stapes.
nuclear complex to the motor nuclei of the trigeminal
The head of the malleus is anchored to the tympanic
and facial nerves (Borg 1973). With electro-acoustic
membrane, whereas the base of the stapes is connected to
7 the vestibular or oval window. Sound waves set the tym-
impedance measurements, stapedius muscle contraction
can be readily detected in response to ipsilateral or con-
panic membrane into vibrating movements, which via
tralateral sound, giving objective information about the
the auditory ossicles are transmitted to the auditory part
functional state of the middle and the inner ear, the
of the inner ear cochlea, a fluid-filled tube that is coiled
auditory and facial nerves and the central auditory
two and a half times. In cross-section, it has a broad base,
pathways in the lower brain stem. Ipsilateral and con-
a pointed apex and a central pillar called the modiolus.
tralateral measurements can distinguish between right,
The bony labyrinth communicates with the tympanic
left and midline lesions of the lower brain stem (Hayes
cavity through two openings in its medial wall, the ves-
and Jerger 1981).
tibular or oval window and the cochlear or round window.
The internal or inner ear consists of a bony and a
The vestibular window is closed by the base of the stapes,
membranous part. The bony labyrinth consists of three
so that vibrations of the auditory ossicles are transmitted
communicating parts in the petrous part of the temporal
to the perilymph of the inner ear. The cochlear window is
bone: the vestibule, continuing anteriorly into the cochlea
closed by the secondary tympanic membrane.
and posteriorly into the semicircular canals (. Fig. 7.2a).
Motion of the auditory ossicles is modified by two
At places, the walls of the vestibule are perforated by sev-
small middle ear muscles, the tensor tympani and the
eral minute foramina, the three maculae cribrosae, supe-
stapedius muscles. The tensor tympani muscle is the larg-
rior, middle and inferior, transmitting the branches of
est of the two. It is attached to the handle of the mal-
the vestibulocochlear nerve (. Fig. 7.2b). The bony
leus and is innervated by the trigeminal nerve. The
labyrinth encloses a corresponding system of membra-
smaller stapedius muscle attaches anteriorly to the head
nous sacs and ducts, the membranous labyrinth, which
of the stapes and is innervated by the facial nerve. The
can be divided into the vestibular labyrinth (the utricle
stapedius and tensor tympani motoneurons form sepa-
and saccule within the vestibule and the three semicircu-
rate cell groups, situated close to the facial and motor

a b

..      Fig. 7.2 The bony labyrinth, a outer view; b inner view. (From ten Donkelaar et al. 2018; courtesy Bob Morreale, Mayo Clinic)
7.2 · The Cochlea and the Cochlear Nerve
377 7
..      Fig. 7.3 The fetal cochlear
duct. At 16 weeks of
development, the cochlear
nerve (cn) fibres pass through a
central pillar, the modiolus
(mod), whereas their cells of
origin form the spiral ganglia
(spg). Below, details of the
spiral organ are shown for 25
weeks of development. bm
basilar membrane, cd cochlear
duct, ihc, ohc inner and outer
hair cells, st scala tympani,
sva stria vascularis, sve scala
vestibuli, tC tunnel of Corti,
tm tectorial membrane,
vm vestibular (Reissner)
membrane. (From ten
Donkelaar et al. 2014)

lar ducts within the semicircular canals) and the cochlear The thickened epithelium that constitutes the spiral
labyrinth, formed by the membranous cochlear duct or organ of Corti can be divided into hair cells, supporting
scala media. The cochlea is composed of three chambers cells and cells of the cochlear duct (. Fig. 7.5). The hair
or scalae: the scala vestibuli, the scala media and the cells are the sensory receptor cells of which there is a
scala tympani, separated from each other by the vestibu- single row of inner hair cells and three rows of outer hair
lar membrane of Reissner and the basilar membrane cells (TNA 2017; Fritzsch and Elliott 2018; ten Donkelaar
(. Fig. 7.3). The inner scala media is filled with endo- et al. 2018). The supporting cells include the inner and
lymph, which is rich in potassium and has the character outer pillar cells of Corti, also known as the rods of
of intracellular fluid. The perilymph of the outer scalae Corti, which are separated by the inner tunnel (the tun-
vestibuli and tympani has approximately the same com- nel of Corti) extending the length of the cochlea, and the
position as the cerebrospinal fluid. The two perilymph inner phalangeal cells and the outer phalangeal cells of
compartments form one space, since they are continuous Deiters. The cells of the cochlear duct include sulcus,
with each other at the apex of the cochlea (the helico- border and glandular cells. The border cells include the
trema). The perilymph drains to the subarachnoid space. inner border cells of Held and the outer border cells of
The scala media or cochlear duct contains the spiral Hensen. Fritzsch and Elliott (2018) also named inner sul-
organ of Corti, which rests on the basilar membrane cus cells and outer sulcus cells (also known as the epithe-
(. Fig. 7.4). The superior wall of the cochlear duct (the lial cells of Claudius), medial and lateral to the inner and
vestibular membrane of Reissner) angles downwards outer border cells, respectively. The outer glandular cells
from lateral to medial, making the cochlear duct wedge- of Boettcher are found between the outer border and
shaped. The lateral wall is the stria vascularis. outer sulcus cells. The hair cells and the supporting and
 378 Chapter 7 · The Auditory System

7.2.2  ochlear Hair Cells: Transduction

C
and Amplification
The human ear can detect sound waves with frequencies
between 20 and 20,000 cycles per second or Hertz (Hz),
i.e. approximately 10 octaves of sound. The human ear
has the greater sensitivity for sounds around 1000 Hz.
The greater the frequency, the higher the pitch. The sound
vibrations that enter the scala vestibuli and the perilymph
at the oval window produce displacement of the basilar
membrane before they finally dissipate back to the mid-
dle ear by movements of the membrane covering the
round window. Transduction of sound occurs in the sen-
sory cells of the spiral organ of Corti. Oscillations of the
basilar membrane produce a shearing force on the stereo-
7 cilia of the receptor cells, which are in firm contact with
the non-oscillating tectorial membrane. The tilting of the
stiff cilia is the adequate stimulus for the auditory recep-
tor cells. The inner and outer hair cells have different roles
in the transduction of energy within the cochlea. Inner
hair cells provide direct input to almost all of the axons in
the cochlear nerve. Their activity is modified by local
amplification of the motion of the basilar membrane pro-
duced by the outer hair cells and hair cell-related sup-
porting cells (Flock et al. 1999; Moore and Linthicum
2004). Several molecules have been identified as having a
vital role in hair cell transduction. They are specifically
expressed in and around the stereocilia and mutations in
their genes lead to deafness (Steel and Kros 2001; Brown
et al. 2008; Kikkawa et al. 2012; ten Donkelaar et al.
..      Fig. 7.4 Photomicrograph of the human cochlea. (From ten
2014; Michalski and Petit 2019). Mice and humans share
Donkelaar et al. 2014; courtesy Jo Curfs, Nijmegen).
a relatively close evolutionary genome, and this makes
mice a crucial model to study the functional genomics of
the auditory system (Brown et al. 2008). The Hereditary
border cells are overlaid by the gelatinous tectorial mem-
Hearing Impairment in Mice website from the Jackson
brane. In humans, there are 12,000 outer hair cells in 3
Laboratory (7 http://hearingimpairment.­jax.­org/index.­
rows at the basal turn, increasing to 4 to 5 rows in the
html) gives an up-to-date overview of all available mouse
second and apical turns, and 3500 inner hair cells in a
models of human hearing disorders, mouse genes and
single row (Retzius 1884; Bredberg 1968; Kimura 1975).
mutations affecting hearing and balance and map posi-
On their apical side, the hair cells contain contractile
tions of these loci on individual chromosomes. The
proteins, including an actin cuticular plate, and about
human counterpart of the website is the Hereditary
100 stereocilia, graded in length, which extend to the
Hearing Loss Homepage (7 http://hereditaryhearingloss.­
overlying tectorial membrane. The stereocilia are com-
org) that presents an up-to-date overview of the genetics
posed of the active contractile proteins actin and myosin
of hearing impairment.
(Flock 1980; Corwin and Warchol 1991). The afferent
fibres from the hair cells pass from the organ of Corti
through small openings in the osseous lamina into the
modiolus. Their cell bodies are located in the modiolus in 7.2.3  piral Ganglion Cells and the
S
the spiral canal of the modiolus (the canal of Rosenthal) Cochlear Nerve: Neural Transmission
as the spiral cochlear ganglion (7 Sect. 7.2.3). The inner
ear is vascularized by the labyrinthine or internal audi- The transition from hair cell activity to neural activity
tory artery, which in some 80% is a branch of the ante- occurs within the cochlea. Activation of the stereocilia
rior inferior cerebellar artery (Kim et al. 1990; Schuknecht results in changes in the intracellular potential that lead
1993). to the release of a neurotransmitter from synaptic vesicle
7.2 · The Cochlea and the Cochlear Nerve
379 7

..      Fig. 7.5 The spiral organ. (After Schuknecht 1993, ten Donke- membrane, 1 inner sulcus cell, 2 inner border cell of Held, 3 internal
laar et al. 2018, and Fritzsch and Elliott 2018). a inner spiral tunnel, phalangeal cell, 4 inner hair cell, 5 inner pillar cell of Corti, 6 outer
b inner tunnel (tunnel of Corti), BM basal lamina, bt basal tunnel pillar cell of Corti, 7, 9 external phalangeal cells (epithelial cells of
fibre (afferent), c outer tunnel (tunnel of Held), CG cochlear gan- Deiters), 8 outer hair cell, 10 outer border cell of Hensen, 11 outer
glion, CN cochlear nerve, id interdental cells, LS limbus spiralis, rt sulcus cell or cuboidal external supporting cell (epithelial cell of
radial tunnel fibre (efferent), SL spiral ligament, SP spiral promi- Claudius), 12 basal external glandular cell (glandular cell of
nence, SV stria vascularis, TM tectorial membrane, VM vestibular Boettcher)

clusters at the base of the hair cells. Opposite such a clus- most apical ganglion cells. In humans, there are about
ter of synaptic vesicles, bulbous nerve terminals are 35,000 spiral ganglion cells (Hinojosa et al. 1985;
found on the outer surface of the cell wall. Six to eight Spoendlin 1985). Two types of ganglion cells are found
such terminals are present on the base of each inner hair (Spoendlin 1985). The majority (90–95%) are type I cells
cell and a smaller number on each outer hair cell (Nadol and contact inner hair cells. The unmyelinated peripheral
1990). These terminals continue as short unmyelinated processes of the remaining ganglion cells (5–10%), the
processes, forming the “dendritic” segment of cochlear type II cells, contact the outer hair cells. The central pro-
nerve fibres. They become myelinated when they enter cesses of both types of ganglion cells form the cochlear
the osseous spiral lamina. Here, they reach their cells of nerve (Spoendlin and Schrott 1989). The cochlear nerve
origin, the spiral ganglion cells (see . Fig. 7.5). The spi- enters the ventral cochlear nucleus on the ventrolateral
ral ganglion extends only halfway from the base of the side of the inferior cerebellar peduncle (see . Figs. 7.8
cochlea to the apex. Therefore, the peripheral processes, and 7.14a, b). Upon entering the brain stem, primary
containing hair cells in the apical and middle turns of the auditory fibres bifurcate into equally sized ascending and
cochlea, extend down through the modiolus to reach the descending branches (Moore and Osen 1979).
 380 Chapter 7 · The Auditory System

7.2.4  he Auditory Periphery: Generation

T such as MS. Acoustic neurinomas may cause complete
of Evoked Activity loss of wave I on the side of the lesion or a significant
increase in the I to III interpeak latency.
Neural activity is reflected in the brain stem auditory
evoked potentials or responses (BAEPS or BAERs), an
externally recordable series of small amplitude and 7.2.5 Hearing Loss
short latency wave-like potentials evoked by a transient
stimulus such as a click (Jewett et al. 1970; Stockard Two types of hearing loss can be distinguished: con-
et al. 1978, 1986). Auditory evoked responses (AERs) ductive and sensorineural. Conductive hearing loss is
can be subdivided according to their latency into brain related to defects in conductive mechanisms in the mid-
stem (ABR), middle latency (MLR) and cortical (ACR) dle ear, resulting from conditions such as otitis media
auditory evoked responses (. Fig. 7.6). In humans, the and otosclerosis. Sensorineural hearing loss is caused by
ABR or BAEP is characterized by six or sometimes disease in the cochlea or its central connection, the
seven deflections (I–VII) in the first 9 msec after the cochlear nerve. Hearing loss of cochlear origin is com-
stimulus. Waves I, III and V are of greatest interest since mon and can result from a variety of conditions,
7 they reflect volume-conducted activity from the levels of including tumours, infections and temporal bone frac-
the acoustic nerve, pons and midbrain, respectively. The tures, or from exposure to excessive noise or ototoxic
earliest BAEP waves (waves I and II) are generated by drugs (Schuknecht 1993). In presbycusis, the hearing
the cochlear nerve, prior to its entrance into the brain loss of the aged, the loss begins with degeneration of
stem (Stockard et al. 1978, 1986; Moller and Jannetta outer hair cells at the basal end of the cochlea, but does
1982; Martin et al. 1995; . Fig. 7.7). A potential cor- not seriously affect hearing until the upper range of
responding to wave II of the scalp-recorded BAEP can speech frequencies, around 3000 Hz, is affected. Noise-
be recorded intrasurgically from the surface of the induced hearing loss and severe blows to the head tend
human cochlear nerve as it passes through the internal to affect the anterior basal turn of the cochlea, the
auditory meatus and crosses the intradural space region that processes 3000–4000 Hz (Moore and
(Martin et al. 1995). This supports an earlier dipole Linthicum 2004). Tinnitus, characterized by noise in
localization study (Scherg and von Cramon 1985).
Therefore, both waves I and II of the human BAEPs are V
generated by activity in axons of the cochlear nerve. 60 dBSL III IV
BAEPs can distinguish between pathologies of the mid- I
II +
C z+(A–)
click
dle and inner ear, the auditory nerve and the brain stem.
There are three major applications of BAEPs in adults: 0.1 V
(1) the detection of tumours in the region of the poste-
rior cranial fossa; (2) evolution of coma; and (3) assess-
ment of patients with suspected demyelinating diseases V

log Ampl ( V) IV
5.0
P2
2.0 III
1.0 Pa P1
IV V
I III II
0.2 II VI
+ P0 +
0.1
– – MGB
0.2 I
N0
Na Nb CI
1.0 N2 II
2.0 N1
SO

5.0 nVIII
1,0 10 50 100 1000 CN 2 4 6 10m
8 10ms
log latency (ms)
ABR MLR ACR ..      Fig. 7.7 Relationship between components of the brainstem
auditory evoked response and the auditory projection pathway. CI
..      Fig. 7.6 Brain stem (ABR), middle latency (MLR) and cortical colliculus inferior, CN cochlear nuclei, ll lateral lemniscus, MGB
(ACR) auditory evoked responses. (From Pasman 1997; courtesy medial geniculate body, nVIII vestibulocochlear nerve, SO superior
Jacko Pasman, Nijmegen) olive, I–V waves of BAEP. (After Stockard et al. 1978)
7.2 · The Cochlea and the Cochlear Nerve
381 7
the ears such as ringing, humming or whistling, is a lateral or bilateral deafness usually accompanied by
common symptom in disorders of the inner ear, but it dizziness or vertigo can be a sign of occlusion of the
can also occur in disorders affecting the eighth nerve basilar artery (Huang et al. 1993; Levine and Häusler
such as an acoustic neurinoma (see 7 Clinical Case 7.1) 2001). Demyelinating disorders may also lead to hear-
and with vertebrobasilar disease. Sudden onset of uni- ing difficulties (see 7 Clinical Cases 7.2 and 7.3).

Clinical Case 7.1 Cerebellopontine Angle Tumour

Electrocochleography and auditory brain stem scanning and MRI demonstrated the presence of a
response (ABR) are important electrophysiological medium-sized cerebellopontine angle tumour in the left
tools for routine use in diagnosing vestibular schwan- ear (. Fig. 7.9a, b). Three years later, she died of meta-
nomas (Eggermont et al. 1980; Chandrasekhar et al. static lung cancer and sepsis. At autopsy, metastases of the
1995). Kaga et al. (1997) reported a case of a vestibular breast cancer were found in the right upper lobe of the
schwannoma, in which electrocochleography and ABR lung and in the right temporal lobe of the brain. The tem-
were correlated with temporal bone pathology. poral bone pathology consisted primarily of a large
Case report: A 74-year-old female presented with a left schwannoma, originating from the left inferior vestibular
hearing impairment. In 1975, she had undergone mastec- nerve and occupying the left internal auditory meatus
tomy of her left breast, and in 1987, at the age of 73, she (. Fig. 7.9c, d). The organ of Corti was well preserved in
was treated with cobalt radiotherapy for a recurrence of each turn. In the modiolus, the numbers of spiral ganglion
the breast cancer. Pure-tone audiometry revealed thresh- cells and cochlear nerve fibres in each turn were decreased.
old elevation in the middle- and high-­frequency range. These histological findings suggest that clear compound
ABR showed no response in the left ear, but electroco- action potentials were recorded from the distal part of the
chleography showed clear compound action potentials. CT cochlear nerve in spite of the presence of the vestibular

a b
nIV

nV1

nV2

nV3

nlll

nVl

nIX
sps
nX

nXI

..      Fig. 7.8 a The course of the vestibulocochlear nerve from nerve, nIV trochlear nerve, nV1 ophthalmic nerve, nV2 maxil-
the inner ear to the brain stem on the right and b the cerebello- lary nerve, nV3 mandibular nerve, nVI abducens nerve, nIX
pontine angle. The black arrow in b points at an acoustic neuri- glossopharyngeal nerve, nX vagus nerve, nXI accessory nerve,
noma and the way it extends (white arrows). nIII oculomotor sps superior petrosal sinus (b after ten Donkelaar et al. 2007)
 382 Chapter 7 · The Auditory System

a c

b d

..      Fig. 7.9 a, b CT and MRI demonstrating the presence of a vestibular schwannoma (HE stain). d Magnification of the ves-
medium-sized tumour in the left internal auditory canal and the tibular schwannoma with mixed Antoni A and B cell types (HE
cerebellopontine angle. c Mid-modiolar section of the left ear stain; from Kaga et al. 1997)
showing enlargement of the internal auditory canal occupied by a

schwannoma. ABR could not be detected because of the 55 Eggermont JJ, Don M, Brackmann DE (1980)
blockade of the proximal portion of the cochlear nerve by Electrocochleography and auditory brainstem
the vestibular schwannoma. electric responses in patients with pontine angle
tumours. Ann Otol Rhinol Laryngol 89:1–19
Selected References 55 Kaga K, Iwasaki S, Tamura A, Suzuki J-I, Haebara
H (1997) Temporal bone pathology of acoustic
55 Chandrasekhar SS, Brackmann DE, Kalpna K,
neuroma correlating with presence of
Devgan KK (1995) Utility of auditory brainstem
electrocochleography and absence of auditory
response audiometry in diagnosis of acoustic
brainstem response. J Laryngol Otol 111:967–972
neuromas. Am J Otol 16:63–67
7.2 · The Cochlea and the Cochlear Nerve
383 7
Clinical Case 7.2 Progress of Adrenoleukodystrophy as Shown by Auditory Brain Stem Evoked Responses

Serial studies of auditory brain stem evoked response ABR was normal at onset but changed to abnormal
(ABR) and slow vertex response (SVR) were obtained patterns. Initially, there was lengthening of the wave V-I
during the progress of adrenoleukodystrophy in a 6-year- interpeak interval. This was followed by the disappear-
old boy who was normal until 5 years of age. His illness ance of the later components as his general condition
began with a gait disturbance, dysarthria and hearing dif- deteriorated. At the terminal stage, only a prolonged wave
ficulty. Later, spastic paralysis, serious deafness and blind- I was recordable (. Fig. 7.10). Postmortem pathology
ness appeared. He died of respiratory failure 2 years after revealed demyelination of the cochlear nerves
onset. (. Fig. 7.11) and marked neuronal loss in the cochlear

..      Fig. 7.10 Progress of LEFT RIGHT

adrenoleukodystrophy. I III V I III V
ABRs from early stage 1
until terminal stage 5.
(After Kaga et al. (1980) 1 JUNE 28’76

2 APR 21’77

3 SEPT29’77

4 DEC 22’77

5 FED 24’78

0.5 µV

2msec

a b

..      Fig. 7.11 Longitudinal sections of a the cochlear nerve and b the facial nerve in a case of adrenoleukodystrophy. (After Kaga
et al. 1980). The auditory nerve is demyelinated, the facial nerve not (Luxol fast-blue-­cresylviolet stain, ×40)
 384 Chapter 7 · The Auditory System

nuclei (see Kaga et al. 1980). In addition, there was a vari- Selected References
ety of extensive degeneration throughout the cerebrum, 55 Kaga K, Tokoro Y, Tanaka Y, Ushijima H (1980) The
the white matter in particular, with secondarily occurring progress of adrenoleukodystrophy as revealed by
neuronal changes. These data suggest that degeneration auditory brainstem evoked response and brainstem
occurred in the brain stem and extended rostrally. histology. Arch Otorhinolaryngol 228:17–27

 linical Case 7.3 Pelizaeus-Merzbacher Disease Showing Only Waves I and II in Auditory Brainstem Responses But Good
C
Auditory Perception

Pelizaeus-Merzbacher disease (PMD), an X-linked reces- them had a normal hearing threshold in pure-tone audi-
sive inheritable disease, manifests itself by dysmyelination ometry and a normal speech discrimination rate in
7 in the CNS and is neuropathologically regarded as a type speech audiometry (. Fig. 7.13). This can be explained
of leukodystrophy. PMD is classified into six types. PMD by a nerve conduction blockade through dysmyelinated
type II is characterized by congenital nystagmus, hypoto- axons or desynchronization of neurons and nerves
nia, rigidity of the trunk and the extremities and mental responsible for the wave following waves I and II.
and speech retardation.
Kaga et al. (2005) followed three young adult males Selected References
with PMD from childhood onwards and later added two 55 Kaga K (2009) Central auditory pathway disorders.
more (Kaga 2009). The patients manifested horizontal Springer, Tokyo
nystagmus and severe rigidity of the extremities. 55 Kaga K, Tamai F, Kodama M, Kodama K (2005)
Although the patients showed only waves I and II in Three young adult patients with Pelizaeus-
auditory brain stem responses (. Fig. 7.12), they had Merzbacher disease who showed only waves I and
relatively good hearing ability at about 30 dB. They II in auditory brainstem responses but had good
could not speak words at all but could hear well and auditory perception. Acta Otolaryngol 125:
enjoyed listening to conversation and music. One of 1018–1023

a b

..      Fig. 7.12 a Auditory brain stem responses of five patients ings of these patients on ENG (time constant 3 msec), showing
with Pelizaeus-Merzbacher disease, in which only wave I or wave typical pendular nystagmus. (After Kaga et al. 2005b)
II are elicited in all cases; b spontaneous eye movement record-
7.3 · The Brain Stem Auditory System
385 7

–20
a –10 b
0
10
20
30
Hearing level (dB)

40
50
60
70
80
90
100
110
120
130
125 250 500 1000 2000 4000 8000
Frequency (Hz)

..      Fig. 7.13 a Pure-tone audiometry showing a normal threshold; b T2-weighted MRI showing a high-­intensity signal in the sub-
cortical area. (From Kaga et al. 2005b)

7.3 The Brain Stem Auditory System cochlear nucleus is layered with molecular, granular and
deep layers. It contains a large variety of cell types and
Upon entering the brain stem, the central processes of is situated dorsolateral to the inferior cerebellar pedun-
the spiral ganglion cells bifurcate and distribute to the cle. The anterior or ventral cochlear nucleus contains
cells of the dorsal and ventral cochlear nuclei (7 Sect. many different cell types and has anterior and posterior
7.3.1). The organization of the terminations was first parts and a cap region. The cochlear nuclei receive a rich
described by Lorente de Nó (1933), based on his Golgi blood supply from branches of the anterior and poste-
studies in a 4-day-old cat. In squirrel monkeys, fibres rior inferior cerebellar arteries (Oas and Baloh 1992).
from the basal turn of the cochlea project to dorsal The secondary auditory projections from the cochlear
regions of the ventral cochlear nucleus, whereas apical nuclei to the superior olivary complex and the inferior
fibres project to ventral regions (Moskowitz and Liu colliculus take various routes (. Fig. 7.14). Ipsilaterally,
1972). The primary cochlear nuclei contribute bilateral a major projection from both ventral and dorsal cochlear
ascending projections to the superior olivary complex nuclei reaches the superior olivary complex (7 Sect.
and to the lateral lemniscus (7 Sect. 7.3.2). The major- 7.3.2). Contralaterally, there are three major ascending
ity of the lateral lemniscal fibres ascend directly to the cochlear projections (Strominger 1973; Strominger et al.
inferior colliculus (7 Sect. 7.3.3). Ascending projections 1977): (1) the largest originates in the ventral part of the
from the inferior colliculus form the brachium of the ventral cochlear nucleus and forms the trapezoid body;
inferior colliculus and reach the medial geniculate body its axons may proceed directly to the contralateral lem-
(7 Sect. 7.4.1), which via the acoustic radiation (7 Sect. niscus or terminate in the superior olivary complex; (2)
7.4.2) projects to the auditory cortex (7 Sect. 7.4.3). fibres from the dorsal part of the ventral cochlear nucleus
form the intermediate acoustic stria; they contribute to
the lateral lemniscus; and (3) a contralateral projection
7.3.1  he Cochlear Nuclei: Diversification
T from the dorsal cochlear nucleus form the dorsal acous-
of Cochlear Input tic stria. The dorsal and intermediate acoustic striae and
the trapezoid body converge to form the lateral lemnis-
The human cochlear nuclei consist of a large anterior or cus. The auditory nuclei do not only serve as relay nuclei
ventral nucleus and a smaller posterior or dorsal nucleus in the ascending auditory projection but also as reflex
(. Fig. 7.14a, b; Moore and Osen 1979; Terr and centres. Efferents from the cochlear nuclei enter the retic-
Edgerton 1985; Adams 1986; Moore and Linthicum ular formation, where they contact neurons, which give
2004; Amunts et al. 2012). The posterior or dorsal rise to the auditory evoked startle reflex.
 386 Chapter 7 · The Auditory System

gtt pt pt

MGB
CS ar

bci
CI
II

SO
7 cn
ct

sad
Cov
Cod

b c d

csp

VTA
csp

nVII rusp
ml
dbc ml
nVIII tsp
ctt
Rm als
NR TP ml PPN
VII Rd
als Cf ll als
Fl Cs IV
ctt KF ll
Vo
Ov Vme
Lc
Cov Pbl
VI Cl
MV icp dlf Pbm

bc
Cod

..      Fig. 7.14 a Overview of the auditory projections in the human liculus inferior, CI colliculus inferior, cn cochlear nerve, Cod, Cov
brain. (After ten Donkelaar et al. 2007); b–d the position of the dorsal and ventral cochlear nuclei, CS colliculus superior, ct corpus
cochlear nuclei (in red), the lateral lemniscus (in light red) and the trapezoideum, gtt gyrus temporalis transversus (gyrus of Heschl), ll
colliculus inferior (in red) in horizontal sections of the brain stem lateral lemniscus, MGB medial geniculate body, pt planum tempo-
(after Duvernoy 1995). ar acoustic radiation, bci brachium of col- rale, sad stria acoustica dorsalis, SO superior olive
7.3 · The Brain Stem Auditory System
387 7
7.3.2  he Superior Olivary Complex:
T neurons in the lateral superior olivary nucleus are tuned
Recreation of Auditory Space to high-­frequency stimuli and are sensitive to interaural
intensity differences. The lateral superior olivary nucleus
The superior olivary complex is the first site for binaural receives a monosynaptic excitatory connection from the
convergence. In primates, the cochlear nuclei project to ipsilateral ventral cochlear nucleus and a disynaptic
the superior olivary complex on both sides of the brain inhibitory connection from the contralateral ventral
stem (Strominger 1973; Strominger et al. 1977). The cochlear nucleus via the peri-olivary nuclei. Since the
superior olivary complex is located in the retropontine dorsal cochlear nucleus does not innervate the superior
tegmentum, lateral to the medial lemniscus and dorsal olivary complex, it is believed not to play a role in the
to the spinothalamic tract. The complex contains the localization of sounds.
medial superior olivary nucleus, the lateral superior oli- Behavioural studies in cats have implicated the supe-
vary nucleus and the peri-olivary nuclei, medial and lat- rior olivary complex in the recreation of auditory space.
eral. Sometimes also a nucleus of the trapezoid body is Cats with lesions above the level of the superior olivary
distinguished (Koutcherov et al. 2004; Paxinos et al. complex, in the lateral lemniscus, the inferior colliculus,
2012). The latter nucleus is indistinct in apes and vesti- the medial geniculate body or the auditory cortex, are
gial in humans (Moore 2000; Moore and Linthicum unable to locate a sound source in the spatial field contra-
2004). The superior olivary complex is important for the lateral to the lesion, whereas cats with lesions below the
localization of sounds (Grothe 2000; Moore and superior olivary complex have more diffuse deficits
Linthicum 2004). A sound is localized by two means (Casseday and Neff 1975; Thompson and Masterton
depending on its frequency: (1) low-frequency sounds 1978; Jenkins and Masterton 1982). A comparable deficit
activate the two ears at somewhat different times (inter- has been observed in human subjects with extensive mid-
aural time differences); (2) high-frequency sounds acti- line lesions of the retropontine tegmentum that elimi-
vate the two ears with somewhat different intensities nated crossed input to the superior olivary complex on
(interaural intensity differences). Neurons in the medial both sides (Griffiths et al. 1997a; Furst et al. 2000; Joris
superior olivary nucleus are tuned to low-frequency and van der Heijden 2019; see 7 Clinical Case 7.4). These
stimuli and are sensitive to interaural time differences. animal and human studies suggest that the auditory spa-
The projection from the ventral cochlear nucleus is tial field is recreated in the brain stem by transformations
thought to contribute to this sensitivity. In contrast, occurring at the level of the superior olivary complex.

Clinical Case 7.4 Impaired Sound Localization Following a Midline Lesion of the Retropontine Tegmentum

In a 45-year-old female patient with an extensive midline and a right hemiplegia that included only the lower face.
lesion of the retropontine tegmentum, eliminating crossed He had no auditory complaints, and his bedside hearing
input to the superior olivary complex on both sides, evaluation was unremarkable. MRI showed a left trape-
Griffiths et al. (1997) observed that the patient had no dif- zoid body infarct, the location of which is indicated in
ficulty in detecting frequency and amplitude modulation . Fig. 7.15a. A year later, he was evaluated with a battery
and no general deficit in detection of auditory temporal of hearing tests. Despite an age-appropriate audiogram
information, but she was unable to determine by sound and normal BAERs, all fusion tests were abnormal for the
alone the location and direction of motion of objects in three stimuli used (clicks, low-pass noise and high-pass
the environment, such as ringing telephones and passing noise) and for interaural time or level disparities
trains. Furst and co-workers analysed sound localization (. Fig. 7.15b). Just noticeable differences were highly
in patients with multiple sclerosis and brain stem infarcts abnormal, and regardless of the size or type of interaural
(Furst et al. 1995, 2000; Aharonson et al. 1998). Levine disparity, the patient indicated that everything sounded as
and Häusler (2001) reported another case (see Case though it were coming from or near the centre of his head
report). (. Fig. 7.15c). Unlike normal subjects, nothing was heard
Case report: An 80-year-old male presented with sud- coming from the far right or left.
den onset of vertigo and vomiting. On examination, he This case is based on a case report by Levine and
was found to have a left gaze palsy, dysphagia, dysarthria Häusler (2001).
 388 Chapter 7 · The Auditory System

a b c Right

V
0.4
IC

Subject response
II
III Centre
Left

µvolts
TB 0.2
SO I
vas Right

Left
0
Co 0 2 4 6 8 ms 7.5 0 7.5
Interaural level difference (dB)

..      Fig. 7.15 a Impaired sound localization in a patient with a lateralization. (After Levine and Häusler 2001; see text for expla-
lesion of the retropontine tegmentum (arrow) involving the trap- nation). Co cochlear nuclei, IC inferior colliculus, ll lateral lem-
7 ezoid body; b brain stem auditory evoked responses; c sound niscus, TB trapezoid body, vas ventral acoustic stria

Selected References and interaural discrimination. Effects of brainstem

55 Aharonson V, Furst M, Levine RA, Chaigrecht M, infarcts and multiple sclerosis lesions. Hear Res 143:
Korczyn AD (1998) Lateralization and binaural 29–42
discrimination of patients with pontine lesions. J 55 Griffiths TD, Bates D, Rees A, Witton C, Golkar A,
Acoust Soc Am 103:2624–2633 Green GGR (1997) Sound movement detection deficit
55 Furst M, Levine RA, Korczyn AD, Fullerton BC, due to a brainstem lesion. J Neurol Neurosurg
Tadmor R, Algom D (1995) Brainstem lesions and click Psychiatry 62:522–526
lateralization in patients with multiple sclerosis. Hear 55 Levine RA, Häusler R (2001) Auditory disorders in
Res 82:109–124 stroke. In: Bogousslavsky J, Caplan LR (eds) Stroke
55 Furst M, Aharonson V, Levine RA, Fullerton BC, Syndromes, 2nd ed. Cambridge University Press,
Tadmor R, Pratt H, et al. (2000) Sound lateralization Cambridge, pp 144–161

7.3.3  he Upper Brain Stem: Integration

T tions arising from the ipsilateral and contralateral
of Ascending Auditory Pathway superior olivary complex; and (3) fibres from the dor-
sal nucleus of the lateral lemniscus. These projections
The lateral lemniscus is clearly visible in the prepontine all pass via the lateral lemniscus. It processes the physi-
tegmentum and the midbrain. Most of its fibres termi- cal characteristics of sounds for auditory perception.
nate in the inferior colliculus. Many of these fibres send In this nucleus, neurons in a single layer are maximally
a collateral branch to the nuclei of the lateral lemniscus, sensitive to similar tonal frequencies. The external
which innervate the inferior colliculus and also directly nucleus is laminated (Geniec and Morest 1971; Amunts
the medial geniculate body. In most mammalian species, et al. 2012) and is also described as external cortex.
the lateral lemniscus contains sizeable ventral, interme- The also laminated pericentral nucleus is also described
diate and dorsal lemniscal nuclei (Moore 1987). In as dorsal cortex and is composed of four layers, I–IV.
humans, only the dorsal lemniscal nucleus is well devel- Lesion studies in cats suggest that the external and
oped (Geniec and Morest 1971; Moore 1987). It gives pericentral nuclei play a role in acousticomotor func-
rise to the commissure of Probst to the contralateral tion such as the orientation of the head and body to
dorsal nucleus. auditory stimuli. The inferior colliculus projects to the
The inferior colliculus is composed of three nuclei: medial geniculate body via the brachium of the infe-
central, external and pericentral. The oval-shaped cen- rior colliculus, which is macroscopically visible on the
tral nucleus is the principal nucleus of the inferior col- lateral surface of the midbrain. The inferior colliculi
liculus and receives input from (1) the direct pathway are interconnected via the commissure of the inferior
from the dorsal and ventral cochlear nuclei; (2) projec- colliculi.
7.4 · The Forebrain Auditory System
389 7
7.3.4  rain Stem Topography: Generation
B the globus pallidus, the caudate/putamen, the amygdala,
of Evoked Potentials the hypothalamus and the thalamus. In line with earlier
tract-tracing studies, pathways to the MGB not only
Waves I and II of the auditory brain stem response are include the inferior colliculus but also the auditory cor-
generated by the cochlear nerve. The subsequent waves tex, the insula, the cerebellum and the globus pallidus
III–VI are generated within the brain stem (see (see Keifer et al. 2015 for further references).
. Fig. 7.7). Intrasurgical recordings made from the sur-
face of the human brain stem and dipole studies suggest
that wave III is generated by a volley of action potentials 7.4.2 The Acoustic Radiation
in axons emerging from the cochlear nuclei in the ventral
acoustic stria (Stockard et al. 1978, 1986; Moller and In 1882, Constantin von Monakow first described the
Jannetta 1982; Scherg and von Cramon 1985). Waves IV origin of the acoustic radiation from the MGB in rabbit
and V are generated further rostrally in the brain stem: experiments. The classic studies in the human brain
wave IV most likely at the level of the superior olivary located the proximal part of the acoustic radiation just
complex contralateral to the stimulated ear, presumably caudal to the thalamus, where it originates from the
by the bend in the axonal pathway occurring at that MGB and then passes through the sublenticular part of
point, and wave V by synaptic activity in the inferior the internal capsule to curve around the inferior sulcus
­colliculus (Moller and Jannetta 1982; Moore et al. 1996). of the insula before reaching the gyrus of Heschl
(Dejerine 1895; Flechsig 1920; Pfeifer 1920). In a more
recent study, Rademacher et al. (2002) showed the ste-
7.4 The Forebrain Auditory System reotaxic localization, intersubject variability and inter-
hemispheric differences of the human acoustic radiation
For decades, the dominant species for research on the (. Fig. 7.16). They showed that the location of the
auditory forebrain has been the cat, but the focus has acoustic radiation varies considerably between individu-
now clearly shifted to non-human primates. Although als and hemispheres. With diffusion-based tractography,
the subcortical auditory systems of monkeys and cats Maffei et al. (2019) found a similar variability.
are largely similar, there are important differences in
cortical organization (Kaas and Hackett 2000).
7.4.3  he Auditory Cortex: Sequential
T
Levels of Auditory Processing
7.4.1 The Auditory Thalamus
The primary auditory cortex (A1) is located on the
The medial geniculate body (MGB) is formed by the transverse temporal gyrus of Heschl in the temporal
medial geniculate nuclei and is clearly visible on the infe- lobe of the cerebral cortex and corresponds to BA41. It
rior surface of the inferior thalamus, lateral to the supe- is surrounded by secondary auditory areas (A2): cau-
rior colliculus (see . Fig. 7.14d). The MGB contains dally the caudomedial area, also known as the temporal
several divisions; the principal auditory relay nucleus is plane or planum temporale, and rostrally the rostral
the laminated ventral or principal medial geniculate area. Geschwind and Levitsky (1968) demonstrated that
nucleus (Winer 1984). It receives the major ascending the temporal plane is larger on the left side in the major-
auditory projection from the central nucleus of the infe- ity of the postmortem brains they examined. Asymmetry
rior colliculus in a precise tonotopic way. In contrast, of the temporal plane may form the substrate for left
the dorsal and medial divisions of the MGB are not lam- hemispheric dominance for language-related auditory
inated and receive much less dense input from the infe- processes (von Economo and Horn 1930; Galaburda
rior colliculus. The ventral medial geniculate nucleus et al. 1978; Geschwind and Galaburda 1985; Ide et al.
projects via the auditory radiation to the tonotopically 1999; Dorsaint-Pierre et al. 2006; Brewer and Barton
organized primary auditory cortex. The dorsal and 2016; Tzourio-Mazoyer and Mazoyer 2017) and is cor-
medial or magnocellular nuclei project to higher-order related with handedness (Steinmetz et al. 1989, 1991).
auditory cortical areas in the temporal plane, areas that The gyrus of Heschl is located largely within the lat-
do not have such a precise tonotopic organization as the eral sulcus (von Economo and Horn 1930; . Fig. 7.17).
primary auditory cortex. The transverse temporal gyrus is often partially dupli-
DTI studies (Devlin et al. 2006; Javad et al. 2013; cated into a double or occasionally triple convexity
Keifer et al. 2015) indicate that the MGB and surround- (Pfeifer 1920; Steinmetz et al. 1989; Penhune et al. 1996;
ing associated areas have a diversity of projections to Leonard et al. 1998; Morosan et al. 2001; Marie et al.
 390 Chapter 7 · The Auditory System

a b

7 ..      Fig. 7.16 The acoustic and optic radiations in coronal a and sagittal b probabilistic maps. (After Rademacher et al. 2002). AR acoustic
radiation, OR optic radiation

2001a, b). The primary auditory cortex was designated

area 41 by Brodmann, TC by von Economo and
Koskinas and KAm and KAlt (medial and lateral audi-
tory koniocortex) by Galaburda and Sanides
(. Fig. 7.18a–c). KAm is the most medial and the most
granular area, whereas the more lateral KAlt is less
granular. Morosan et al. (2001) suggested three areas
with well-developed layers IV, Te1.1, Te1.0 and Te1.2, to
represent the primary auditory cortex (. Fig. 7.18d).
There is considerable variability in size of the auditory
koniocortex, and its extent does not coincide with gyral
or sulcal anatomy (Galaburda and Sanides 1980;
Rademacher et al. 1993, 2001a, b; Hackett et al. 2001;
Morosan et al. 2001). The human auditory koniocortex
(BA41/TC/KA/Te) is homologous to the core area of
the monkey auditory cortex. Based on parvalbumin
staining, Wallace et al. (2002) suggested that the gyrus
of Heschl contains two core fields, partially surrounded
by at least six belt fields that lie mostly on the superior
..      Fig. 7.17 The human auditory cortex. The primary auditory cor-
temporal gyrus. In an fMRI study, Wessinger et al.
tex is composed of two fields, TD and TC. On the right side (R),
these occupy a double transverse temporal gyrus (Heschl gyrus); on (2001) showed that pure tones primarily activate the
the left side (L), they correspond to a single Heschl gyrus and a part core and that more complex sounds activate belt areas.
of the more caudally situated planum temporale (PT). TD and TC The primate auditory core area is located in the centre
are composed of markedly granular subareas (dotted in red) and less of the superior temporal plane (Hackett et al. 2001;
granular areas. Note the distinct right-left asymmetries with a larger
. Fig. 7.19). In primates, a centrally located core region
planum temporale on the left side. A anterior, HG Heschl gyrus, P
posterior, TA superior temporal area, TB magnocellular supratem- containing two or three subdivisions including the pri-
poral area, TC transverse supratemporal area, TD intercalate supra- mary auditory area (A1), a surrounding belt of cortex
temporal area, TG temporopolar area. (After Brodal 1981) with some seven divisions and a lateral parabelt region
comprised of at least two fields have been described. In
2015; Tzourio-Mazoyer and Mazoyer 2017). The cyto- monkeys, the core region can be identified on the basis of
architecture of the human auditory cortex has been specific anatomical and physiological features. The region
described by Brodmann (1908, 1909), von Economo and shows dense immunostaining for parvalbumin in layer
Koskinas (1925), Galaburda and Sanides (1980) and IV, surrounded by a more lightly stained belt, which is
more recently Hackett and co-workers (Hackett et al. flanked by a very sparsely stained parabelt (Jones et al.
2001; Hackett and Kaas 2004) and Rademacher and 1995; Kosaki et al. 1997). Parvalbumin staining also
colleagues (Morosan et al. 2001; Rademacher et al. marks the human core auditory cortex in humans
7.4 · The Forebrain Auditory System
391 7

a b c d
TA1
T 1
TA
Tpt Te2
T 2
Te
22 PaAc /d
TBmp paAe
TBma TTe1.1
42
TD paAl
KAlt Pa Ar
TC
41 KAm Te1.0
T 1.0
Te
TB
P roA
ProA
52 Te1.2
T
PaAl
22 TA2
T 2
TA

TG1 TG2

38 T 3
Te
Te3

..      Fig. 7.18 Regional parcellation of the right human superior nal, lateral and rostral auditory parakoniocortex, ProA proauditory
temporal cortex (rostral is below) according to a Brodmann, b von cortex, TA1, TA2, TB, TBma, TBmp, TC, TD subdivisions by von
Economo and Koskinas, c Galaburda and Sanides and d Morosan Economo and Koskinas, Te2, Te1.0, Te1.1, Te1.2, Te3 subdivisions
and co-workers. (After Hackett and Kaas 2004 and Morosan et al. by Morosan and co-workers, TG1, TG2 temporopolar subdivisions
2001). In a–c, core areas are shown in red, belt areas in medium red of von Economo and Koskinas, Tpt temporoparietal area, 22, 38,
and parabelt areas in light red. Kalt, Kam lateral and medial auditory 41, 42, 52 Brodmann areas
koniocortex, PaAc/d, paAe, PaAl/paAl, PaAr caudal/dorsal, exter-

(Nakahara et al. 2000; Wallace et al. 2002; Chiry et al. The human auditory koniocortex is surrounded ros-
2003). In macaque, chimpanzee and human brains, trally, laterally and caudally by an area of parakoniocor-
Hackett et al. (2001) identified the auditory core from tex (. Fig. 7.18). This region covers the lateral part of
serial sets of adjacent sections processed for cytoarchitec- the transverse temporal gyrus and extends rostrally and
ture, myeloarchitecture, acetylcholinesterase and cyto- caudally over the superior temporal plane. The auditory
chrome oxidase. The position of the core region with parakoniocortex has been called area 42 by Brodmann
respect to major sulci and gyri in the superior temporal and TB by von Economo and Koskinas. Galaburda and
region varied most in chimpanzee and human brains. Sanides (1980) distinguished three regions: (1) a rostral
In monkeys, most neurons of the ventral division of auditory parakoniocortex (PaAr) on the rostral aspect
the MGB project to the core cortex (Mesulam and of the superior temporal plane; (2) a lateral, internal
Pandya 1973; Burton and Jones 1976; Luethke et al. auditory parakoniocortex (PaAl), lateral to A1; and (3)
1989; Rauschecker et al. 1997). These thalamocortical a caudal auditory parakoniocortex (PaAc), covering the
projections terminate in layers IV and lower III in regu- caudal portion of the superior temporal plane and
lar patches of higher density label, separated by areas of extending around the insula to the parietal operculum.
less dense labelling (Pandya and Rosene 1993; Hashikawa In its turn, the parakoniocortex is surrounded by an
et al. 1995). In contrast, the medial and dorsal divisions extensive area of auditory cortex that covers the remain-
of the MGB project to the core area diffusely. It seems ing of the superior temporal plane and the lateral sur-
likely that the human primary auditory cortex also face of the superior temporal gyrus, except for its rostral
receives dense thalamic input. This input explains the pole. This region corresponds to BA22, TA of von
cochleotopic organization shown in this area by func- Economo and Koskinas (1925) and the external audi-
tional imaging, including MEG (Elberling et al. 1982; tory parakoniocortex (PaAe) by Galaburda and Sanides
Hari et al. 1989; Pantev et al. 1995; Lutkenhoner and (1980).
Steinstrater 1998), PET (Lauter et al. 1985; Ottaviani In primates (. Fig. 7.19), anatomical and physio-
et al. 1997; Lockwood et al. 1999), fMRI (Wessinger logical studies defined a belt area surrounding the core
et al. 1997; Scheich et al. 1998; Di Salle et al. 2001) and rostrally, laterally and caudally (Pandya and Sanides
microelectrode mapping studies in epilepsy patients 1973; Galaburda and Pandya 1983; Morel and Kaas
(Howard et al. 1996). 1992; Morel et al. 1993; Hackett et al. 1998a). The area
 392 Chapter 7 · The Auditory System

cs
cs ips ips
as
as
Tpt
ps CM
h
ps
CL I
IN AI h lus
RM I h lus
RTM R I ML CPB
RT
h I I CPB
AL RPB
h
RTL
RPB ls
vbls STG
STG

sts sts

..      Fig. 7.20 Topography of auditory-related projections. Caudal

..      Fig. 7.19 Auditory and auditory-related cortices in macaque (CPB) and rostral (RPB) subdivisions of the parabelt and the supe-
7 monkeys. Core areas (A1, R, RT) are shown in red, belt areas (CL,
CM, AL, RM, RTL, RTM) in medium red and parabelt areas (CPB,
rior temporal gyrus (STG) project topographically to segregated
regions of superior temporal, posterior parietal and prefrontal corti-
RPB) in light red. Major sulci have been opened to show the extent ces. as arcuate sulcus, cs central sulcus, ips intraparietal sulcus, ls
of auditory-­related cortex. A1 primary auditory area, AL anterolat- lateral sulcus, lus lunate sulcus, ps principal sulcus, sts superior tem-
eral area, as arcuate sulcus, CL, CM caudolateral and caudomedial poral sulcus, Tpt temporoparietal area. (After Hackett and Kaas
areas, CPB caudal parabelt area, cs central sulcus, h, l high and low 2004)
frequencies, IN insula, ips intraparietal sulcus, lus lunate sulcus, PL
posterolateral area, ps principal sulcus, R rostral area, RM rostro-
medial area, RPB rostral parabelt area, RT rostrotemporal primary
auditory cortex, RTL, RTM lateral and medial rostrotemporal areas, nine dye DiI. With DTI, the tracts connecting the gyri
STG superior temporal gyrus, sts superior temporal sulcus, vbls ven- of Heschl via the corpus callosum have been studied
tral bank of lateral sulcus. (After Hackett et al. 2001) (Hofer and Frahm 2006; Westerhausen et al. 2009).
These interhemispheric connections are located more
rostral and lateral to the belt is nowadays known as the rostrally within the posterior callosal third than those
parabelt (Morel et al. 1993; Hackett et al. 1998a). Both connecting the posterior parts of both superior tempo-
belt and parabelt areas differ from the core area in their ral gyri.
pattern of thalamic input. The macaque belt area The idea of a two-stream, what/where organization
receives projections from only the medial and dorsal of sensory cortex originated in the visual system (see
divisions of the MGB (Rauschecker et al. 1997), whereas Chap. 8). In rhesus monkeys, such a dichotomy has also
the parabelt area is also innervated by these two divi- been demonstrated for the cortical auditory projections
sions of the MGB but, moreover, by the medial division (Rauschecker and Tian 2000). The “where” (dorsal)
of the pulvinar (Trojanowski and Jacobson 1975; Burton pathway is thought to link A1 via the caudomedial belt
and Jones 1976; Hackett et al. 1998b). to the frontal eye field and parietal targets (Romanski
Ablation of the core of macaque auditory cortex et al. 1999; . Fig. 7.20) that are implicated in spatial
eliminates responses to auditory stimuli in the adjacent processing. The “what” (ventral) pathway is thought to
belt region (Rauschecker et al. 1997), suggesting that represent a pattern information stream that originates in
input from the medial and dorsal geniculate nuclei is not the anterior core and belt areas and influences targets
sufficient to support auditory processing in the absence within the temporal lobe. A similar two-stream organi-
of direct projections from the ventral geniculate nucleus. zation may exist in the human auditory cortex (Griffiths
Instead, information processing to the secondary audi- et al. 2000; Alain et al. 2001; Maeder et al. 2001;
tory cortical areas appears to depend on transcortical Wessinger et al. 2001; Clarke et al. 2002). The right
projections that pass successively from core to belt to insula is activated by a moving sound image (Griffiths
parabelt cortex (Jones and Powell 1970; Seltzer and et al. 1994), and, conversely, a patient with a right hemi-
Pandya 1978; FitzPatrick and Imig 1980; Luethke et al. spheric stroke causing atrophy of the right insula was
1989; Morel and Kaas 1992; Morel et al. 1993; Hackett unable to detect sound source movement by either phase
et al. 1998a). Tardif and Clarke (2001) studied the or loudness cues (Griffiths et al. 1996). Subjects listening
intrinsic connectivity of human auditory areas with to stimulus movement stimulated by changes in binaural
anterograde and retrograde labelling of the carbocya- timing show maximal activity in the inferior parietal
7.4 · The Forebrain Auditory System
393 7
area, particularly on the right side (Griffiths et al. 1998; wards and caudalwards on the superior temporal plane.
Weeks et al. 1999). These findings suggest (1) that there The area of activation is generally within and around the
is a transcortical passage of information from auditory transverse temporal gyrus. With exposure of subjects to
koniocortex mediocaudalwards across the insula into more complex stimuli such as passive listening to tone
the parietal lobe, during processing of information on patterns, single words, pseudowords or narrative text,
sound source position and motion (see Hackett and activity is not only present in the cortex of the superior
Kaas 2004), and (2) a dominant functional role of the temporal gyrus, but now foci of activation appear on the
right hemisphere in sound localization. lateral aspect of the superior temporal gyrus in BA22/TA/
In functional imaging studies, simple auditory tasks, PaAc (Binder et al. 1994). The human primary auditory
such as passive listening to white noise bursts, tones or cortex is functionally organized in a tonotopic manner. In
consonant-vowel speech syllables, activate restricted areas a combined fMRI and DTI study, Upadhyay et al. (2007)
within the lateral sulcus on the superior temporal plane showed that the connectivity pattern in the human pri-
(Zatorre et al. 1992, 1994; Binder et al. 1994, 1997, 2000; mary auditory cortex is similar to that described in tono-
Zatorre and Binder 2000). The extent of the activation topic mapping studies on macaque monkeys (Morel et al.
varies from subject to subject and may spread rostral- 1993) and cats (Lee et al. 2004; Lee and Winer 2005).

Clinical Case 7.5 Middle-Latency Auditory Evoked Magnetic Fields in Patients with Auditory Cortex Lesions

The generators of auditory middle-latency responses at 0.96 ms intervals based on the magnetic field data
(AMLRs) have been a subject of controversy. The conven- obtained at each measurement point. ECDs are a collec-
tional MLR, which is recorded from the patient’s scalp, is a tion of hypothetical dipoles that would produce the pat-
far-field recording of electric potential differences gener- tern of the magnetic field recorded at a particular point in
ated by neural currents. The signal is significantly affected time. Typical normal recordings are shown in . Fig. 7.21a,
by the intervening tissues, such as the scalp, cranial bones in which the ECD is superimposed on the brain MRI scan.
and cerebrospinal fluid. Also, multiple generators cannot The ECD is localized in the auditory cortex in the right
be isolated in such recordings. In contrast, in magnetoen- and left hemispheres (. Fig. 7.21b).
cephalography (MEG) the magnetic field generated by the Left auditory cortex lesions: . Fig. 7.22a, b shows
electric current in neurons is measured. As the magnetic MLAEFs and the dipole localization fitted to an MRI for
permeability of the intervening tissue is almost the same as a typical patient, a 65-year-old male.
that of air, the magnetic field can be measured on the sur- Right auditory cortex lesions: . Fig. 7.22c, d shows
face of the scalp with little distortion. MEG is particularly AMLRs and MLAEFs and the dipole localization fitted to
effective in localizing signals from axons that are oriented an MRI for a typical patient, a 63-year-old male. Compared
perpendicular to the scalp as those in the cortex and its pro- to the Pa component of the AMLR, the Pam of the
jections. MEG is suited for the precise localization of the MLAEF is substantially more sensitive to activity of the
activity sources in the brain. As an indicator of auditory auditory cortex ipsilateral to the magnetic sensor. The pri-
cortex function in MEG, the N1m is widely used in basic mary generator of the Pam in MLAEFs has been demon-
and clinical studies. There have been only a few studies of strated to be the auditory cortex. However, the Pa of
the Pam of middle-latency auditory-evoked magnetic fields AMLRs is evoked only partly from the auditory cortex
(MLAEFs), which are localized in the auditory cortex, and because it is evoked even in patients with unilateral audi-
no auditory cortex lesion study of the Pam of MLAEFs. tory cortex lesions.
MLAEFs were recorded in a magnetically shielded
room using a 37-channel SQUID gradiometer (Magnes;
Selected References
Biomagnetic Technologies). The patient was recumbent on
a bed with his/her head fixed by a vacuum cushion. 55 Kaga K, Kurauchi T, Yumoto M, Uno A (2004)
Auditory stimulation was provided by tone bursts Middle-latency auditory-evoked magnetic fields in
(2000 Hz; 100.2 dB perSPL; rise/fall time 0.1 ms; plateau patients with auditory cortex lesions. Acta Otolaryngol
10 ms). Equivalent current dipoles (ECDs) were estimated 124:376–380
 394 Chapter 7 · The Auditory System

a b

0 50 100 150 msec

7 c
Right hemisphere Light hemisphere
Pa Pa

Pam EEG(Cz) Pam

MEG

0.5 µV
50fT
10msec

..      Fig. 7.21 a Comparison of AMLR wave with superimposi- typical simultaneous recordings of AMLRs and MLAEFs in a
tion of all MLAEFs recorded from the entire scalp in a normal normal subject, a 25-year-old male; right- and left-hemispheric
control; b superimposition of the ECD on the auditory cortex of recordings were made with contralateral stimulation. (From
an MRI; a white circle indicates the localization of the ECD; c Kaga et al. 2004)

a b
Right hemisphere Light hemisphere

C3

CZ

C4

MEG

0.5 µV
50fT
10msec
c d
Right hemisphere Light hemisphere

C3

CZ

C4 Pam
MEG

0.5 µV
50fT
10msec

..      Fig. 7.22 a AMLRs and MLAEFs and b MRIs of a 64-year- persists bilaterally; (c, d) ibid., of a 63-year-old male patient with
old male patient with a left auditory cortex lesion as part of a a right auditory cortex lesion as part of a temporoparietal infarc-
temporoparietal infarction; the MLAEF is absent from the left tion; the MLAEF is absent from the right hemisphere, but the
hemisphere but present from the right one, whereas the AMLR Pam is present from both hemispheres. (From Kaga et al. 2004)
7.4 · The Forebrain Auditory System
395 7
In general, activity is bilaterally equal. With com- ral cortical areas. Cortical deafness is characterized by
plex stimuli, language in particular, the question arises bilateral abolition of the middle and late latencies of
whether there is a right-left asymmetry in the response. auditory potentials, caused by bilateral lesions of the
Since handedness influences hemispheric lateralization, primary auditory cortices. Such patients have the feel-
imaging studies of speech processing are normally ing of being deaf to all types of auditory stimuli, but
restricted to neurologically normal right-handers. In often say they are not deaf, rather than they do not
them, there is a tendency for greater activation of the understand what is said to them. The term subcortical
left hemisphere during tasks that depend on word deafness is used to indicate an auditory disorder clini-
meaning. Left lateralization of speech characterizes cally identical to cortical deafness but due to lesions in
both males and females (Frost et al. 1999). The func- subcortical areas of the brain. It was first described by
tional significance of greater left hemispheric activity is Le Gros Clark and Russell (1938). The ischaemic
implied by imaging studies of stroke patients after lesions involved the two external capsules and extended
infarctions of the left perisylvian area (Weiller et al. sufficiently downwards to interrupt the acoustic radia-
1995; Heiss et al. 1997; Mummery et al. 1999). Subjects tions while sparing the auditory cortices. Recent cases
who showed good recovery of speech perception had were reported by Woods (1996), Levine and Häusler
increasing activation of the left temporal cortex sur- (2001) and Kaga et al. (2005a; see 7 Clinical Cases 7.6
rounding the infarct. Some indications for an opposite and 7.7).
asymmetry in processing musical stimuli come from Since the pioneering studies of Ferrier (1875) and
cases of pathology: Henschen (1920), there has been a long-standing debate
1. A patient with a right thalamic tumour experienced as to whether bilateral destruction of either the primary
distorted perception of music but not of voices auditory cortex or the acoustic radiation results in audi-
(Roeser and Daly 1974). tory agnosia. In macaque monkeys, bilateral lesions of
2. Cortical activity has been demonstrated in the right the primary auditory cortex apparently do not cause
superior temporal lobe during musical hallucinations permanent deafness (Heffner and Heffner 1990). Less
(Kasai et al. 1999). recovery of function in the human brain, compatible
3. A case of amusia, a form of auditory agnosia, was with the clinical diagnosis of auditory agnosia, may or
seen after an infarct involving the right insula may not have been caused by the inclusion of the sur-
(Griffiths et al. 1997b). rounding auditory association areas (Lechevalier et al.
2007).
Tanaka et al. (1991) differentiated three clinical
7.4.4 Auditory Disorders Related to Stroke syndromes of auditory agnosia: (1) disconnection syn-
dromes, destroying the acoustic radiation and causing
Disorders of auditory perception may follow strokes auditory agnosia (prephonemic deficit); (2) cortical
in the territory of the internal carotid arteries or of the lesions of the left superior temporal lobe, which may
vertebrobasilar system (Levine and Häusler 2001; result in pure word deafness (linguistic deficit); and (3)
Lechevalier et al. 2007; Kaga 2009) and appear as: unilateral or bilateral temporoparietal or subcortical
1. Auditory agnosia, the impossibility of recognizing lesions, which have been documented in patients with
environmental sounds, words and music which the non-verbal auditory agnosia (deficit to environmental
patient, however, is said to hear sounds). Lesions occurring peripherally to the MGB
2. Pure word deafness, the impossibility to understand (prethalamic) may cause hearing loss and those bilat-
spoken language to repeat or to write under dicta- erally located centrally to the MGB (postthalamic)
tion in the absence of other signs of aphasia may result in auditory agnosia. Small lesions of the
3. Cortical deafness, the feeling of being deaf contrast- MGB may be related to auditory hallucinations
ing with the integrity of the tonal audiogram (Fukutake and Hattori 1998). Pure word deafness may
4. Amusia, auditory agnosia specific for music be the result of left or bilateral temporal lesions, pos-
sibly due to disconnection as suggested by Liepmann
The central disorders of auditory perception may and Storch (1902). Recent cases were reported by
result from lesions of either the right, the left or both Kaga et al. (2000; see 7 Clinical Case 7.8) and Levine
cerebral hemispheres, usually involving parietotempo- and Häusler (2001).
 396 Chapter 7 · The Auditory System

Clinical Case 7.6 Cortical Deafness

A right-handed 38-year-old man’s complete loss of hear- perception and speaking ability but preserve inner speech.
ing was diagnosed as cortical deafness caused by bilateral Brain imaging showed extensive bilateral infarction of the
cerebral vascular lesions in the auditory cortices. primary auditory cortex and the auditory radiation and
Neurological examination showed loss of somatosensory localized bilateral infraction of the postcentral gyrus and,
sensation with normal motor function and articulation partially, of the third frontal gyrus (. Fig. 7.24).On the
ability. Pure-tone audiometry of both ears revealed off- basis of the clinical data, a neuropsychological diagnosis
the-scale results, and speech audiometry demonstrated 0% of cortical deafness was made, with loss of vestibular and
maximum speech discrimination (. Fig. 7.23a). However, somatosensory sensations and anarthria. In the National
objective audiometry showed normal distortion product Institute of Sensory Organs of the National Tokyo
optoacoustic emissions (DPOAE) and normal auditory Medical Centre, he underwent training for lip-reading to
brain stem response (ABR; . Fig. 7.23b, c). The patient aid his communication, but his learning was poor.
showed 0% perception of environmental, speech and music Presently, he communicates by writing only.
sounds in both ears. He was unable to feel vestibular sensa-
7 tion despite normal caloric nystagmus. He showed no
Selected References
damage to his larynx or articulation organs.
A neurological test revealed systematic loss of somato- 55 Kaga K, Shinjo Y, Enomoto C, Shindo M (2015) A
sensory sensation of temperature, pain, touch and vibra- case of cortical deafness and loss of vestibular and
tion with normal motor function. An intellectual function somatosensory sensations caused by cerebrovascular
test revealed a PCRM score of 30/30. A memory test lesions in bilateral primary auditory cortices, auditory
showed only mild visual memory impairment. The stan- radiations, and postcentral gyruses – complete loss of
dard aphasia test revealed normal reading and writing hearing despite normal DPOAE and ABR. Acta
abilities. However, he showed complete loss of auditory Otolaryngol 135:389–394

a -20
-10
0
10
20
30
Hearing level (dB)

40
50
60
70
80
90
100
110
120
130
(dB) 125 250 500 1000 2000 4000 8000 (Hz)
Frequency (Hz)

b c

..      Fig. 7.23 a Pure-tone audiometry in a case of cortical deafness; b, c ABRs. (From Kaga et al. 2015)
7.4 · The Forebrain Auditory System
397 7

..      Fig. 7.24 MRIs showing bilateral cerebrovascular lesions in a case of cortical deafness. Flair images reveal bilateral lesions in
the auditory cortex, radiation and postcentral gyrus and partial damage of the inferior frontal gyri. (From Kaga et al. 2015)

Clinical Case 7.7 Auditory Agnosia Caused by Bilateral Lesions Restricted to the Auditory Radiations

Bilateral lesions of the auditory radiations are rare bilateral increase in blood flow in the auditory cortex in
(Tanaka et al. 1991; Woods 1996; Kaga et al. 2005; see response to both click and monosyllable stimuli. This may
Case report). be due to activation of the auditory cortex via non-­specific
Case report: Kaga and co-workers reported a patient pathways.
with auditory agnosia due to bilateral lesions of the audi-
tory radiations (Kaga et al. 2005). A 43-year-­ old male
Selected References
patient experienced mild left temporal hemiplegia due to a
right putaminal haemorrhage. He recovered completely, but 55 Kaga K, Kurauchi T, Nakamura M, Shindo M, Ishii
hypertension persisted. When he was 53 years old, he had a K (2005) Magnetoencephalography and positron
left putaminal haemorrhage and went into a coma. After emission tomography studies of a patient with audi-
recovering from the coma and the right hemiplegia, he could tory agnosia caused by bilateral lesions confined to the
hear but could not discriminate speech sounds. Brain CT auditory radiations. Acta Otolaryngol 125:1351–1355
and MRI demonstrated small bilateral lesions restricted to 55 Tanaka Y, Kano T, Yoshida M, Yamadori A (1991)
the auditory radiations (. Fig. 7.25a, b). Pure-tone audio- “So-called” cortical deafness. Clinical, neurophysi-
grams recorded 1 and 4 years after the second haemorrhage ological and radiological observations. Brain 114:
are shown in . Fig. 7.25c, d. Magnetoencephalography 2385–2401
demonstrated the disappearance of middle latency responses 55 Woods RP (1996) Correlation of brain structure and
and AEP studies showed a very small Pa peak. In contrast, function. In: Toga AW, Mazziotta JC (eds) Brain map-
a positron emission tomographic study showed a marked ping: the systems. Academic, San Diego, pp 365–402
 398 Chapter 7 · The Auditory System

a b

c d
–20 –20
–10 –10
0 0
10 10
20 20
30 30
Hearing level (dB)
Hear ing level (dB)

40 40
50 50
60 60
70 70
80 80
90 90
100 100
110 110
120 120
130 130
125 250 500 1000 2000 4000 8000 125 250 500 1000 2000 4000 8000
Freguency (Hz) Freguency (Hz)

..      Fig. 7.25 Auditory agnosia caused by bilateral lesions by small brain infarcts. Pure-tone audiograms recorded one c
restricted to the auditory radiations. In the axial a and coronal b and four d years after the second haemorrhage. (From Kaga et al.
MRIs, the auditory radiations are bilaterally damaged (arrows) 2005a)

Disorders of music perception following cerebral 2. A pure amusia, where only music perception is
damage can be divided into two categories (Lechevalier affected (for congenital amusia see Ayotte et al. 2000;
et al. 2007): Peretz 2016; Wang et al. 2017)
1. Multimode perceptive disorders affecting more or
selectively musical sounds but with verbal and envi- In both monkeys and humans, neurons in core areas
ronmental sound difficulties respond strongly to narrowband sounds such as tones,
7.4 · The Forebrain Auditory System
399 7
whereas neurons in belt areas respond better to more com- Neuropsychological studies in epileptic patients who
plex sounds such as noise (Wessinger et al. 2001; underwent a unilateral temporal cortectomy have con-
Rauschecker and Tian 2004; Tian and Rauschecker 2004; tributed to our knowledge of the localization of musical
Bendor and Wang 2006). Within the core areas, two mirror functions (Liégeois-Chauvel et al. 1998). A right tempo-
symmetric tonotopic maps sharing a low-­frequency border ral cortectomy was found to disturb melodic perception
have been identified, corresponding to A1 and the rostral as well as the perception of pitch intervals, whereas a
field R (Formisano et al. 2003; Bendor and Wang 2006; left-sided lobectomy did not disturb perception of the
Brewer and Barton 2016). In monkeys, a third core area intervals. These data underline the key role of the supe-
(RT) has been found that lies rostral to R (Kaas and rior temporal gyrus in discrimination of melodies.
Hackett 2000; Hackett and Kaas 2004). Kaas and Hackett Cortectomy of the posterior part of T1, including the
postulated that each core area is connected to medial and temporal plane, the lateral part of the Heschl gyrus and
lateral neigbouring belt areas (see . Fig. 7.17), with addi- BA22, is more striking for the processing of pitch and
tional belt areas located on the rostral and caudal ends of variations of rhythm than cortectomy of the rostral part
the core. Three of these lateral belt areas (caudal-lateral, of T1. Disorders of the perception of rhythm and metre
middle-lateral and anterolateral) have been mapped elec- (recognition of a cadence of march or waltz) can be dis-
trophysiologically and possess similar mirror tonotopic sociated. The right and left rostral parts of T1 would be
maps to those of their adjacent core (Rauschecker and implicated in the processing of metre. Griffiths et al.
Tian 2004; Tian and Rauschecker 2004). In an fMRI study, (1997b) reported a patient with lesions of the middle and
Patterson et al. (2002) identified a specific region in the lat- posterior temporal areas and the insula of the right
eral part of the gyrus of Heschl that was preferentially acti- hemisphere. The patient complained of not being able to
vated by temporally regular sounds with a pitch. They appreciate music. Neuropsychological testing showed a
determined that only lateral Heschl gyrus, a non-primary deficit of musical perception without disturbance of the
auditory region rostrolateral to the primary auditory cor- perception of noises, environmental sound and speech
tex, responded to the temporal regularity of pitch of the sounds. His ability to detect continuous changes of
acoustic stimuli. Other imaging studies (Penagos et al. sound frequency was preserved. However, a disturbance
2004; Schneider et al. 2005) have confirmed these findings. in the analysis of rapid sequences of notes seemed to be
Musical perception is not a uniform competence in the the basis of his musical perception deficit. Neuroimaging
general population. Some patients will have had musical studies have revealed that rhythm perception activates
training, others not. Peretz (2001) estimated that 5–10% BA44 and that detection of pitch changes relies on the
of individuals are completely unable to distinguish the left cuneus and precuneus (Platel et al. 1997, 2003).
pitches of two notes of music or to memorize the smallest Auditory hallucinations are observed in brain stem
musical tone. Geschwind and Galaburda (1985) suggested (Ross et al. 1975; Cambier et al. 1987; Fisher and Tapia
that rightward deviation from the usual pattern of cere- 1987; Griffiths 2000) and temporal lobe (Lechevalier
bral asymmetry may be associated with increased gifted- et al. 1985) strokes. Cambier et al. (1987) reported five
ness for talents for which the right hemisphere is assumed purely auditory observations of hallucinosis (hallucina-
to be important. With MR morphometry, Schlaug and tions, regarded by the patient as abnormal), four of
co-workers presented evidence for structural brain asym- which were attributed to paramedian strokes of the pons
metry in musicians (Schlaug et al. 1995). Musicians with and one to an infarct of the dorsolateral mesencepha-
perfect pitch revealed stronger leftward asymmetry of the lon. Auditory hallucinations following temporal lobe
planum temporale than nonmusicians or musicians with- lesions are unusual and have specific characteristics
out perfect pitch. This suggests that outstanding musical (Liepmann and Storch 1902; Lechevalier et al. 1985;
ability is associated with increased leftward asymmetry of Augustin et al. 2001; Evers and Ellger 2004; Sacks 2007;
the cortex subserving music-related functions. see 7 Clinical Case 7.9).

Clinical Case 7.8 Neuropathology of Auditory Agnosia Following Bilateral Temporal Lobe Infarction

Severe auditory deficits due to bilateral lesions of the pri- 1975 when the patient was 37 years old. He was admitted to
mary auditory cortex or the auditory radiations is very hospital for examination following his second cerebrovascu-
rare. The resulting hearing problem is referred to as audi- lar accident. MRI of the lesions at admission is shown in
tory agnosia or cortical deafness. Kaga and co-­workers . Fig. 7.26a, b. A comprehensive follow-up examination of
reported a patient who came to autopsy (Kaga et al. 2000; auditory function was periodically conducted until his sud-
see Case report). den death 15 years later. His brain was studied neuropatho-
Case report: Kaga’s case of auditory agnosia due to logically. Initial pure-tone audiometry revealed moderate
bilateral lesions of the auditory cortex was first diagnosed in sensorineural hearing loss in the right ear and mild sensori-
 400 Chapter 7 · The Auditory System

a b

..      Fig. 7.26 Auditory agnosia following bilateral temporal lobe part of the lateral sulcus, whereas in the left hemisphere exten-
infarction. a, b Axial (here the left side is on the left) and coronal sive infarction can be seen in Broca’s area, the superior temporal
(here the left side is on the right) MRIs showing a large infarct in gyrus and the supramarginal gyrus. d, e HE-stained sections of
the left hemisphere and a small infarct in the right hemisphere the medial geniculate body (MGB). In the left MGB, neurons
including the auditory cortex. c Lateral views of the brain and have been completely replaced by glial cells d, whereas in the
two horizontal sections in which the auditory cortex is present. right MGB e there is partial neuronal preservation. (From Kaga
In the right hemisphere, a small infarct is present in the upper et al. 2000)
7.4 · The Forebrain Auditory System
401 7

d e

..      Fig. 7.26 (continued)

neural hearing loss in the left ear. Repeated pure-tone audi- tre of the superior temporal gyrus and partial gliosis of the
ometry revealed that bilaterally thresholds became MGB were found (. Fig. 7.26c, e). These data support the
progressively poorer over time. Speech audiometry of both clinical observations of imperception of speech sounds,
ears consistently revealed that the patient was unable to dis- music and environmental sounds, which may be due to pro-
criminate any monosyllabic words. In general, speech and gressive degeneration of both MGBs.
hearing tests demonstrated that he could not comprehend
spoken words but could comprehend written commands and
Selected References
gestures. Neuropathological examination of the brain
revealed a total defect and neuronal loss of the superior tem- 55 Kaga K, Shindo M, Tanaka Y, Haebara H (2000) Neu-
poral gyrus, including the gyrus of Heschl, and total gliosis ropathology of auditory agnosia following bilateral
of the medial geniculate body (MGB; . Fig. 7.26c, d). In temporal lobe lesions: a case study. Acta Otolaryngol
the right hemisphere, subcortical necrosis, gliosis in the cen- 120:259–262

Clinical Case 7.9 Auditory Hallucinations Following a Metastasis in the Gyrus of Heschl

Case report: A 64-year-old patient presented with word- non-fluent with word-finding difficulties and suboptimal
finding difficulties. He suffered from coronary sclerosis comprehension. On hospital admission, he repeatedly
with exercise-induced angina pectoris, but he had no pre- complained of auditory hallucinations, consisting of
vious neurological complaints. On neurological examina- incomprehensible words and sounds. On MRI, a con-
tion, there were no focal signs, but his speech was trast-enhancing lesion was found in the left gyrus of
 402 Chapter 7 · The Auditory System

a b

..      Fig. 7.27 a Axial and b coronal T1-contrast MRIs of a metastasis in the left gyrus of Heschl that caused auditory hallucinations.
(Courtesy Peter van Domburg, Sittard-Geleen)

Heschl (. Fig. 7.27) that appeared to be part of a more cytoma for which he was treated with radiotherapy and
lobular contrast-­enhancing in the left parietotemporal temozolomide.
region with surrounding oedema. The auditory hallucina- This case was kindly provided by Peter van Domburg
tions disappeared on treatment with dexamethasone. A (Department of Neurology, Zuyderland Medical Centre,
biopsy showed that the tumour was a gemistocytic astro- Sittard-Geleen, Netherlands).

7.5 The Descending Auditory System tory nerve fibres in the region of the inner hair cells
(Liberman and Brown 1986; . Fig. 7.28). Most of the
Parallel with the pathways from the spiral organ of fibres of the olivocerebellar bundle decussate in the
Corti to the auditory cortex, there is an uninterrupted tegmentum. They enter the vestibular nerve and join
chain of neurons conducting impulses in the opposite, the cochlear nerve via the vestibulocochlear anasto-
descending direction. The final link in this descending mosis of Oort (Schuknecht 1993) to terminate in the
auditory system is formed by the olivocochlear bundle inner and outer hair cells of the spiral organ of Corti.
of Rasmussen, which originates in the peri-olivary The human olivocochlear system has been identified
nuclei around the superior olivary nucleus as two with acetylcholinesterase histochemistry (Schuknecht
components: larger myelinated fibres from medial et al. 1959) and choline acetyltransferase immunohis-
nuclei to the outer hair cells and small unmyelinated tochemistry (Moore et al. 1999; Moore and Linthicum
fibres from the lateral nuclei to the dendrites of audi- 2004).
References
403 7
..      Fig. 7.28 Efferent control of ohc ihc
the cochlea. Cod, Cov dorsal
and ventral cochlear nuclei, ct
corpus trapezoideum, ihc inner Cod
hair cells, ll lateral lemniscus,
ocb olivocochlear bundle, ohc ocb II
outer hair cells, PON periolivary SO
Cov
nuclei, SO superior olivary
complex. (After Nieuwenhuys
1984)
PON
ct

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