Translational Perspectives in Auditory Neuroscienc... - (7. The Superior Olivary Complex)

7
The Superior Olivary Complex

Shigeyuki Kuwada and Tom C. T. Yin
fibers from the cochlea. As both cochlear nuclei

Learning Objectives impinge upon cells in the SOC, it represents the ini-
tial site of binaural interaction. The SOC is so named
n The reader will be able to describe the because anatomically it is in a superior position rel-
anatomic divisions of the superior olivary ative to the inferior olivary complex. The term oli-
complex (SOC). vary is based on the olive-shaped protuberance on
n The reader will be able to describe the the ventral lateral surface of the medulla created by
binaural cues and neural circuitry used by the underlying inferior olivary complex. The SOC
neurons in the SOC to localize sounds extends from the rostral medulla to the caudal pons
n The reader will be able to describe the and is called a complex because it represents many
anatomic pathways linking the SOC to nuclear groups. The SOC can be functionally divided
the cochlear nuclei, lateral lemniscus, and into a feedback system to the cochlea (olivocochlear
inferior colliculus. system), an inhibitory periolivary system and a
n The reader will be able to describe the sound-localization system. Anatomically, there is
frequency bias of the medial superior olive considerable overlap between these systems. The
and the lateral superior olive. SOC varies in size and composition among species
(Figure 7–1). The main nuclei, the lateral (LSO) and
Key Words. Superior olivary complex, lateral medial (MSO, Figure 7–1, green filled) superior oli-
superior olive, medial superior olive, medial vary nuclei can usually be identified in most species,
nucleus of the trapezoid body, periolivary nuclei, but the nuclei that surround the LSO and MSO, viz.,
medial olivocochlear system, lateral olivocochlear the periolivary nuclei (Figure 7–1, gray filled), take
Copyright © 2012. Plural Publishing, Inc.. All rights reserved.
system, interaural time differences, interaural many forms. The tuning of neurons in LSO is biased
intensity differences, sound localization towards high frequencies, whereas those in the
MSO are biased towards low frequencies (Guinan
et al., 1972). Thus, the relative size of the LSO and
MSO reflect the animal’s frequency range of hear-
Functional Anatomy of the
ing (Glendenning & Masterton, 1998). So, animals
Superior Olivary Complex
with a hearing bias towards high frequency sounds
(e.g., mice and rats) have a large LSO and a small
The superior olivary complex (SOC) is an important MSO. Animals with good low and high frequency
relay center for ascending auditory information as hearing (e.g., cats) have a prominent LSO and MSO.
it receives projections from the cochlear nucleus, Humans have a hearing bias toward low frequency
which in turn is the destination of all auditory nerve sounds so the most prominent nucleus is the MSO.
163
Tremblay, Kelly. Translational Perspectives in Auditory Neuroscience : Normal Aspects of Hearing, edited by Robert F. Burkhard, Plural Publishing, Inc., 2012. ProQuest Ebook Central,
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164 Translational Perspectives in Auditory Neuroscience: Normal Aspects of Hearing
(SPON) although they are not entirely equivalent in

their inputs and outputs. The MNTB is classically
considered a main nucleus but we include it with
the periolivary group because it logically fits with
this group. The trapezoid body (aka, ventral acoustic
stria) is a thick band of axons bounded ventrally by
the ventral border of the brainstem and the pyrami-
dal tract and the approximate position of the dorsal
border is shown in Figure 7–2B. The trapezoid body
is primarily made up of axons of cochlear nucleus
(CN) neurons projecting to the SOC, axons from
SOC nuclei to other SOC nuclei, and axons from SOC
nuclei projecting to higher structures. The trapezoid
body is so named because the descending axons
from the abducens (cranial nerve VI) nucleus create
an image of a trapeze with the descending abducens
nerve fibers being the ropes of the trapeze and the
crossing axons the seat or body of the trapeze.
Feedback System to the Cochlea

(olivocochlear system)
Our treatment of this system is brief because it is

comprehensively discussed by Guinan (see Chapter
Figure 7–1. The superior olivary complex in different spe-
cies. Lateral superior olive (LSO), medial superior olive 11). This is a feedback system where neurons in the
(MSO), medial nucleus of the trapezoid body (MNTB). SOC project their axons to the hair cells of the cochlea,
Based on Schwartz, 1992. Mouse and rat provided by Tet- hence the name olivocochlear system. A major role
sufumi Ito. of this system is to actively alter the mechanical tun-
ing of the basilar membrane by affecting the motility
of the outer hair cells (OHCs). This system is often
The LSO in humans is difficult to identify and even referred to as a cochlear amplifier.
more difficult is the medial nucleus of the trapezoid Figure 7–2 shows the locations of olivocochlear
body (MNTB), a periolivary nucleus that has strong neurons that were stained by injecting a retrograde
projections to the LSO in most mammals (Bazwinsky tracer, into the left cochlea of a cat (Vetter et al., 1991;
et al., 2003). Warr et al., 2002). Two populations of neurons can be
Figure 7–2 shows the organization of the SOC in seen, those located medial and those located lateral
the cat from its caudal (Figure 7–2A) to rostral (Fig- to the MSO and are appropriately named the medial
ure 7–2D) extent. The main nuclei of the SOC, the (MOC) and lateral (LOC) olivocochlear neurons.
MSO and LSO, are depicted as green and the perioli- The LOC neurons can be further divided into those
vary nuclei as gray. The periolivary nuclei surround that are in close proximity to the margins of the LSO
the main nuclei and are named according to position: (marginal LOC) and those located more distally to
medial (MNTB), ventral (VNTB), and lateral (LNTB) the LSO (para-LOC). The olivocochlear neurons
nuclei of the trapezoid body and the anterior lateral project bilaterally, however, MOC neurons project
(ALPO), dorsal lateral (DLPO), and dorsal medial predominantly to the contralateral cochlea whereas
(DMPO) periolivary nuclei. In rodents the DMPO those in the LOC project primarily to the ipsilateral
nucleus is called the superior paraolivary nucleus cochlea.
Figure 7–2. Transverse sections depicting the caudal (A) to rostral (D) extent of the SOC. Also depicted in the cen-
ter is a line drawing of the whole brainstem at that level of the SOC. The main nuclei, medial superior olive (MSO)
and lateral superior olive (LSO) are colored green. The periolivary nuclei, medial (MNTB), ventral (VNTB) and lat-
eral (LNTB) nuclei of the trapezoid body and the anterior lateral (ALPO), dorsal lateral (DLPO), and dorsal medial
(DMPO) periolivary nuclei are colored gray. Also shown at the rostral extreme is the ventral nucleus of the lateral lem-
niscus (VNLL). Adapted from Warr et al., 2002, with permission by the Association for Research in Otolaryngology.
165
Figure 7–3 provides a schematic of the olivoco- Sobkowicz, 1989). About two-thirds of the neurons
chlear system. The MOC neurons are myelinated and project to the contralateral cochlea and one-third to
innervate the base of OHCs using acetylcholine as its the ipsilateral cochlea. In the cat, the MOC neurons
transmitter (Vetter et al., 1991), although a small pro- almost exclusively reside in three periolivary nuclei,
portion may use GABA as a transmitter (Whitlon & VNTB, MNTB, and DMPO. These neurons show
Figure 7–3. Schematic of olivocochlear system. medial olivocochlear (MOC), lateral olivocochlear (LOC), outer hair cell
(OHC), inner hair cell (IHC), tectoral membrane (TH), pyramidal tract (PT). Adapted from Warr et al., 2002, with permis-
sion by the Association for Research in Otolaryngology.
The Superior Olivary Complex 167
sharp frequency tuning and project to many hair al., 1991) are found to colocalize with acetylcholine.
cells located above and below the frequency tuning The LOC neurons receive inputs from the ipsilateral,
of the MOC neuron (Liberman & Brown, 1986). The posteroventral cochlear nucleus (PVCN: Warr, 1982).
marginal cell region of the anteroventral cochlear
nucleus (AVCN) project bilaterally to MOC neurons.
It is hypothesized that the marginal cells provide
information about sound intensity as part of a feed-
Inhibitory, Periolivary System
back gain control system comprising the cochlea,
cochlear neurons, CN, MOC neurons, and cochlear This system does not appear to have a unitary func-
OHCs (Ghoshal & Kim, 1997; Ye et al., 2000). tion and is, as a whole, the least understood group
The function of the LOC neurons is not well of nuclei of the SOC. A common feature is that most
understood because their small size and unmyelin- periolivary neurons are immunoreactive for glycine
ated axons make recordings difficult. In cat, cell bod- and GABA. Thus, these neurons provide inhibitory
ies of LOC neurons are preferentially distributed in inputs to the CN (Figure 7–4) as well as to other
the low frequency region (lateral limb) of the LSO. nuclei of the SOC. In general, the role of inhibition
They project to the inner hair cells (IHCs) where they in sensory systems is to sharpen receptive fields,
synapse on the afferent terminals of auditory nerve enhance contrast and improve frequency tuning.
fibers (Liberman, 1980). This projection appears tono- Also shown in Figure 7–4 is the projection of MOC
topic, because injections of anterograde tracers at neurons to the contralateral VCN. As described (see
progressively more medial regions of the LSO label Figures 7–2 and 7–3), these neurons use acetylcho-
terminals near IHCs at progressively more basal line as a transmitter. The periolivary nuclei, except
locations in the ipsilateral cochlea (Guinan et al., for the MNTB, show dense immunoreactive label-
1984). LOC neurons use acetylcholine as a transmit- ing for serotoninergic fibers (Figure 7–5). Serotonin
ter, but other neuroactive substances (enkephalin, is considered a neuromodulator and is produced in
Altschuler et al., 1984; dynorphin, Abou-Madi et al., the Raphe nucleus, a structure that runs the length of
1987; and calicitonin gene-related peptide, Vetter et the brainstem. Serotonin levels are low during sleep
Figure 7–4. Outputs of periolivary nuclei to cochlear nuclei. Adapted from Helfert and
Aschoff, 1997, with permission by the Oxford University Press, Inc.
and high during vigilant states. A local injection of rons of the inferior colliculus, though the effect can
serotonin usually usually depresses responses and be stimulus dependent (Hurley & Pollak, 1999).
increases neural response latencies to sound in neu- Another common feature is that the perioli-
vary nuclei receive their excitatory input from the
CN (Figure 7–6). These inputs are from specific cell
types (octopus, globular bushy and stellate cells) in
the VCN. The collateral branches in the schematic of
Figure 7–6 are not necessarily meant to indicate that
the same cell in the CN innervates different perioli-
vary nuclei, though most cells do innervate more
than one target, but instead that the same cell type
can innervate more than one periolivary nucleus.
The MNTB and VMPO receive inputs from the con-
tralateral VCN, the DLPO, and LNTB from the ipsi-
lateral VCN, and the DMPO and VNTB from both
VCNs (see review by Helfert & Aschoff, 1997).
In addition to the inputs to the SOC from the
cochlear nuclei, higher-order structures also provide
inputs to the SOC. Figure 7–7 shows these descending
inputs. The heaviest projections are from the thalamus
and inferior colliculus (IC), with a lighter projection
Figure 7–5. Distribution of immunoreactive serotonergic from the auditory cortex (Thompson & Schofield, 2000).
fibers in the SOC of the cat. Reprinted from (Thompson and Interestingly, the DMPO and VNTB are the major recip-
Schofield, 2000), with permission by Microscopy Research ients of these inputs and they are the only periolivary
Techniques (John Wiley & Sons). nuclei that receive input from both CN (see Figure 7–6).
Figure 7–6. Cochlear nucleus inputs to periolivary nuclei. Adapted from Helfert and
Aschoff, 1997, with permission by the Oxford University Press, Inc.
The VNTB houses many MOC neurons and in Figure 7–8. Both of the neurons display suppres-
many of these neurons are excited by binaural sion to a 50-msec tone burst at high and low sound
sound stimulation, consistent with the inputs from levels, followed by a punctuate but long-lasting off
both CN. MOC neurons exhibit a slow chopping response. The rate-level function of these two neu-
firing pattern that persists for the duration of the rons (panels C & F) indicates that the off-response is
sound (Liberman & Brown, 1986). In contrast, the monotonic over a wide intensity range (~60 to 70 dB).
predominant response of DMPO/SPON neurons Humans are sensitive to even a wider range, but the
is suppression to sound stimulation followed by a range seen in these off neurons is 2 to 3 times greater
robust off-response when the sound is turned off than that seen in the auditory nerve. Although the
(Kulesza et al., 2003; Kuwada & Batra, 1999). These response to tones is suppressive, periodic sinusoi-
neurons have a strong preference to sounds pre- dal amplitude modulated (SAM) tone can entrain
sented to the contralateral ear. As described above, the off-response to create a time-locked response to
DMPO/SPON neurons receive an excitatory input the modulation frequency. Figure 7–9 (left column)
from octopus cell in the contralateral CN as well as shows the response of a SOC neuron in the form of
a weak input from stellate cells in the ipsilateral CN.
This structure also receives a strong projection from
the ipsilateral MNTB that uses the inhibitory trans-
mitter, glycine. So, the suppression seen to contra-
lateral sound stimulation is most likely created by
the MNTB input, and release from inhibition, that
is, at sound offset, creates an off response through a
rebound mechanism (Kuwada & Batra, 1999). Exam-
ples of off-responses recorded in or near the vicinity
of the DMPO in the unanesthetized rabbit is shown
Figure 7–8. Examples of SOC neurons that show an off

Figure 7–7. Schematic of major descending projections response to tone bursts and their rate-level functions to the
to the SOC. Adapted from Thompson and Schofield (2000), off response. Adapted from Kuwada and Batra (1999), with
with permission by Microscopy Research Techniques (John permission by the Society for Neuroscience via Copyright
Wiley and Sons). Clearance Center.
Figure 7–9. Response of an off-neuron to SAM tones. Left column: post-stimulus time histograms to modu-
lation frequencies between 25 and 800 Hz. Right column: corresponding cycle histograms binned over a cycle
of the modulation frequency. Carrier frequency = 6 kHz, intensity = 42 dB SPL. Adapted from Kuwada and
Batra (1999), with permission by the Society for Neuroscience via Copyright Clearance Center.
170
poststimulus time histograms to different modula- lation frequency, even at the highest modulation
tion frequencies. At 800 Hz, there is a weak sustained frequency where the sustained response is weak.
response during the 1100 msec SAM tone followed Careful analysis of the phase indicates that the sus-
by a robust off-response. However, at progres- tained response is due to the entrainment of the neu-
sively lower modulation frequencies, the sustained ron’s off response (Kuwada & Batra, 1999). As shown
response becomes more robust and the off response in Figure 7–9, this off response is present over a wide
at the lowest modulation frequencies (50 and 25 Hz) range of modulation frequencies, and is also respon-
blends completely with the sustained response. The sive over a wide range of sound levels and modula-
cycle histograms created by averaging the response tion depths. An example is shown in Figure 7–10.
over one cycle of the modulation frequency (right When synchrony is measured, the modulation trans-
column) only over the stimulus duration indicate fer function to sound intensity (Figure 7–10A) and to
that the spike timing is highly locked to the modu- modulation depth (Figure 7–10C) both show primarily
Figure 7–10. Modulation transfer functions (MTFs) of an off-neuron as a function of sound level and modulation depth.
MTFs based on synchrony (A) and spike rate (B) at different sound levels. MTFs based on synchrony (C) and spike rate (D)
at different modulation depths measured at 50 dB SPL. E. Synchrony as a function of level and modulation depth measured
at 100 Hz modulation. F. Spike rate as a function of level and modulation depth measured at 100 Hz modulation. Adapted
from Kuwada and Batra (1999), with permission by the Society for Neuroscience via Copyright Clearance Center.
a low-pass shape. When measured as a function of

intensity or modulation depth (at 100 Hz modula- Sound Localization System
tion) synchrony becomes asymptotic (Figure 7–10E).
In contrast, the spike rate modulation transfer func- The ability to localize sounds in space is accom-
tions to intensity and depth is primarily band pass in plished by comparing the signals at the two ears.
shape. The spike rate is non-monotonic with sound The comparison can be in the difference in the time
level and monotonic with modulation depth (Figure of arrival of the signals at the two ears, viz., inter-
7–10F). A common view of the role of inhibition is aural time differences (ITDs), or in the difference in
that it attenuates or suppresses post-synaptic neu- sound pressure level of the signals at the two ears,
ral activity. Although this is true for off neurons, the viz., interaural level differences (ILDs). The SOC is
robust discharge when inhibition is released adds considered to be the initial site where these binaural
a new dimension. For simple sounds, (e.g., tones), comparisons are made. Chapter 14 discusses bin-
the off response can code a wide range of sound aural hearing, and specifically sound localization,
levels (see Figure 7–8). For complex sounds, the off in more detail). Figure 7–11 displays these binaural
response becomes entrained to each modulation, cues measured with miniature microphones placed
resulting in precise temporal coding of the envelope deep in the rabbit’s ears to a broad band sound from
(see Figures 7–9 and 7–10) 5 locations along the horizontal plane in an anechoic
Off responses in the SOC of rats are almost chamber. The traces in the upper panel for each loca-
exclusively found in the SPON (Kulesza et al., 2003). tion display the time waveforms recorded at each
Unlike the robust off response seen in the unanesthe- ear, whereas the lower panel displays the response
tized rabbit (e.g., see Figure 7–8), the off responses in in the frequency domain. For any source off the mid-
the anesthetized rat often constitutes a single action line, the sound will reach the closer ear first, creating
potential. Neurons in the DMPO and SPON project an ITD. Because the head is an obstacle to sound,
to the ipsilateral IC using GABA as a transmitter the sound at the closer ear will also be louder than
(Saldana & Berrebi, 2000). The role of this projection that to the distal ear, creating an ILD. The degree to
is unclear but would serve to modulate AM sensitiv- which a sound is attenuated by striking an object,
ity or be a source of AM processing in the midbrain. like a head, depends upon the wavelength of the
Kadner and Berrebi (2008) have suggested that off sound relative to the size of the object. If the wave-
neurons may play a role in gap detection. length is long with respect to the size of the head,
then there is minimal attenuation and therefore
small ILD. If the wavelength is short (i.e., high fre-
Question 1 quency) relative to head size, then there is large
attenuation and large ILD. This dependence of ILD
on frequency can be clearly seen in the frequency
Are there diseases known to result in disor-
response traces of Figure 7–11, that show increasing
dered processing in the human SOC?
divergence of the left and right ear traces as a func-

tion of frequency. It follows that ILDs are an impor-
Answer 1 tant cue to localize high-frequency sound sources. In
contrast, ITDs are an important cue to localize low
Diseases like multiple sclerosis do target
frequency sound sources because the neural tim-
myelinated fibers and the SOC receives
ing information needed to convey ITDs is present
inputs from large myelinated axons. How-
in auditory nerve fibers, only for frequencies below
ever, this disease has wide spread effects
~2 kHz. This dichotomy between the mechanisms
and would not specifically target the SOC.
for localizing low- and high-frequency signals was
Vascular strokes in this area of the brainstem
formulated long ago (Rayleigh, 1907) and is often
are often fatal so again deficiencies specific
referred to as the Duplex theory. Interestingly, the
to the SOC would not be reported.
main nuclei of the SOC, the LSO and MSO, can be
Figure 7–11. Acoustic recordings made in the ear canals of a rabbit to a broad band sound from 5 different spatial loca-
tions along the horizontal meridian. Upper panels depict the time waveform from the left (blue) and right (red) ear and
corresponding lower panels depict the power spectrum.
viewed as the structural basis for the Duplex the- hand, there is the opposite bias in the MSO with a
ory: ITDs are encoded in the MSO whereas ILDs are disproportionate representation of low frequencies
encoded in the LSO. and neurons sensitive to ITDs.
The frequency dichotomy expressed in the The inputs to the MSO and LSO are illustrated
Duplex theory is reflected in the distribution of best in Figure 7–13. The MSO receives excitatory (gluta-
frequencies in the MSO and LSO. As can be seen in matergic) inputs from spherical bushy cells in the
Figure 7–12, both the LSO and the MNTB have a VCN of both sides (see Figure 7–13A). In addition it
disproportionate number of neurons tuned to high also receives inhibitory (glycinergic) inputs from the
frequencies in accord with the role of the LSO for ipsilateral LNTB and MNTB that may be the source
encoding ILDs (Guinan et al., 1972). On the other of ipsilateral- and contralateral-induced inhibition,
dreau & Tsuchitani, 1970). As expected, the recep-

tive fields of LSO cells are such that they respond to
stimuli in the ipsilateral sound field and are turned
off by sounds in the contralateral sound field.
Processing of ITDs
In order for a neuron to encode ITDs, the inputs from

each ear must reflect the temporal structure of the
sound waveforms at each ear. For tonal sounds, this
feature is called phase-locking. Phase-locking begins
to roll off around 1 kHz in most species. The excep-
tion is the barn owl where phase-locking is seen to
~9 kHz. The frequency limits of phase-locking dic-
tates the frequency limit for ITD sensitivity. So, for
most mammals with low frequency hearing, the
bulk of the neurons prefer ITD at frequencies below
~1.5 kHz, but can extend to 2 to 3 kHz in the cat. The
Figure 7–12. Tonotopic organization of the LSO, MSO, and barn owl can show ITD sensitivity to about 10 kHz.
MNTB in the cat. Based on Guinan et al. (1972) and Bou- In humans, the limit is about 1.1 kHz.
dreau and Tsuchitani (1970). The type of ITD sensitivity is dependent on
whether the inputs from each ear are excitatory
or inhibitory. Figure 7–14 represents the predicted
response of a MSO (see Figures 7–15A and 7–15B)
respectively, since globular bushy cells provide excit- or LSO (see Figures 7–14C and 7–14D) neuron to
atory input to the ipsilateral LNTB and contralateral low frequency tonal stimulation that arrive in-phase
MNTB (Smith et al., 1991; Cant & Hyson, 1992). (Figures 7–14A and 7–14C) or out-of-phase (Figures
The LSO receives excitatory input from spheri- 7–14B and 7–14D) between the ears. The inputs to
cal bushy cells in the ipsilateral cochlear nucleus (see these neurons have action potentials that are tempo-
Figure 7–13B). The input from the contralateral CN rally locked to the tonal waveform and this feature
originates from globular bushy cells whose axons is referred to as phase-locking (Joris et al., 1994). The
cross the midline and synapse onto principal cells in MSO neuron receives phase-locked excitatory inputs
the MNTB with one of the most remarkable synapses (see Figure 7–14, column 2) from either ear and the
in the brain: the giant calyces of Held (Tolbert et al., LSO neuron (see Figures 7–14C and 7–14D) receives
1982). In turn, the axons of the principal cells in the excitatory input from the ipsilateral ear and inhibi-
MNTB make inhibitory glycinergic (Moore & Cas- tory input from the contralateral ear (re: to the side of
pary, 1983) synapses onto LSO neurons of the same the LSO cell). Shown for both the MSO and LSO are
side (Spangler et al., 1985). In rat, another source of cases when the ITD is such that the inputs from each
inhibitory input to the LSO is from the contralateral ear arrive coincident in time (in-phase, see Figures
VNTB (Warr & Beck, 1996). Planar multipolar cells 7–14A and 7–14C) or when they arrive maximally
in the DCN may also project to the ipsilateral LSO in discordant in time (out-of-phase, see Figures 7–14B
the rat (Doucet & Ryugo, 2003). The result of these and 7–14D). For the model MSO neuron, the phase-
inputs is that LSO cells are excited by stimulation of locked, action potentials from each ear evoke phase-
the ipsilateral ear and inhibited by stimulation of the locked, excitatory postsynaptic potentials (EPSPs,
contralateral ear, so-called IE cells, thereby making see Figure 7–14, column 3). In contrast, for the LSO
them sensitive to the ILD between the two ears (Bou- neuron, the phase-locked, action potentials from the
Figure 7–13. Schematic of the medial superior olive (MSO) circuit (A) and the lateral
superior olive (LSO) circuit (B). Abbreviations: dorsal (DCN) and ventral (VCN) cochlear
nucleus, spinal trigeminal tract (STT), medial (MNTB), ventral (VNTB), and lateral (LNTB)
nuclei of the trapezoid body (TB), dorsal lateral (DLPO) and dorsal medial (DMPO) peri-
olivary nuclei, pyramidal tract (PT).
contralateral ear evokes phase-locked, inhibitory each other and no action potentials are discharged.
postsynaptic potentials (IPSPs) and those to ipsilat- In the case where the inputs arrive discordant in
eral stimulation evoke phase-locked EPSPs. For the time, the model MSO neuron is minimally excited
MSO neuron, when the inputs arrive coincident in (see Figure 7–14B) whereas the model LSO neuron
time (see Figure 7–14A), the EPSPs from each side is maximally activated (see Figure 7–14D, column 4
optimally sum, creating suprathreshold EPSPs (see and 5). When the ITD is systematically varied, the
Figure 7–14A, column 4) and a maximal discharge ITD functions for the model MSO and LSO show a
of action potentials (see Figure 7–14A, column 5). cyclic function at the period of the stimulating fre-
Under the same conditions for the model LSO neu- quency (see Figure 7–14, column 6). At maximum
ron (see Figure 7–14C), the EPSPs and IPSPs cancel coincidence (0 ITD) the MSO neuron fires maximally
Figure 7–14. A neural schema of ITD processing for model MSO and LSO neurons. The MSO neuron (A and B) receives
excitatory (+) inputs from each side, and the LSO neuron (C and D) receives excitatory inputs from the ipsilateral side and
inhibitory inputs (-) from the contralateral side. Column 1: 5 cycles of a low frequency tone delivered to the contralateral
(blue trace) and ipsilateral (red trace) ear either in-phase (A & C) or out-of-phase (B & D). Column 2. Schematic of action
potentials (spikes) phase locked to the stimulating tone that synapse onto a MSO (A & B) or LSO (C & D) neuron. Column 3.
Postsynaptic potentials evoked by the contralateral and ipsilateral phase locked spikes. Column 4. Summed postsynaptic
responses to binaural stimulation. Threshold for action potentials is indicated by arrows and is lower in the LSO cell (C &
D) than for the MSO cell (A & B). Column 5. Schematic of the spike output as a result of the summed postsynaptic poten-
tials exceeding action potential threshold. Column 6. Schematic of the ITD functions for the model MSO and LSO when
the ITD is systematically varied.
whereas the LSO neuron fires minimally. Note that multiple frequencies should show alignment of the
at maximal activation the MSO neuron exceeds its maximum discharge (peak) for MSO neurons and
monaural inputs whereas the maximum response of alignment of the minimal discharge (trough) for LSO
the LSO neuron does not exceed its ipsilateral input. neurons. This prediction is illustrated in Figure 7–15.
As the ITD function is cyclic when the ITD of a For the model MSO neuron (Figure 7–15A ), the ITD
tone is varied (see Figure 7–14, column 6), it is not functions at different stimulating frequencies (500
possible to determine whether coincidence evokes to 1500 Hz) show a peak discharge that align at a
maximum excitation or suppression using a single common ITD, in this case, when the ipsilateral tone
tonal stimulus. If the mechanism proposed in Fig- is delayed by 150 µsec relative to the contralateral
ure 7–14 is operating, then the ITD functions across tone. In contrast to the model MSO neuron, the
Figure 7–15. Schematic of a peak (A–C) and a trough (D–F) type neuron. A and D. ITD functions across frequency for
a peak and trough type neuron, respectively. B and E. Composite curve derived from averaging the functions in A and D.
C and F. Linear fit of mean interaural phase versus stimulus frequency for a peak and trough type neuron. Characteristic
phase (CP) is the phase intercept at 0 Hz and the characteristic delay (CD) is the slope of the linear fit.
ITD functions for the model LSO neuron display a CD reflected a difference in the anatomical delays
minimum (trough) at a common ITD, in this case, required to activate the binaural cell. By offsetting
when the ipsilateral stimulus is delayed by 150 µsec the difference in anatomical delays with an ITD, the
(Figure 7–15D). The middle panels (Figures 7–15B inputs from each ear would arrive simultaneously at
and 7–15E) show the composite curves derived by the binaural neuron and maximally excite or inhibit
averaging the ITD functions in the corresponding it. The quantitative analysis of CDs was developed
panels. The composite curve for the MSO neuron later by Yin and Kuwada (1983) and is illustrated
has a peak at 150 µsec whereas that for the LSO in the right panels (see Figures 7–15C and 7–15F).
neuron has a trough at 150 µsec. The alignment of The mean interaural phase for maximal discharge
the peaks or troughs of the ITD functions was first for each ITD curve is plotted as a function of stimu-
observed in the IC by Rose et al. (1966), and the ITD lating frequency and fitted with a linear regression
where this alignment occurred was called the “char- line. The slope of the regression line represents the
acteristic delay” (CD). They hypothesized that the CD, and the y-intercept at 0 Hz is the characteristic
phase (CP). For the model MSO neuron, a CP of 0 or neuron recorded in the cat (Tollin & Yin, 2005; Yin &
equivalently 1 cycle indicates that the CD occurred Chan, 1990). Like the model neurons, the peak of the
at maximal discharge (see Figure 7–15C), while for a ITD functions across frequency align at the same ITD
model LSO neuron a CP of 0.5 cycles indicates that for the MSO neuron, whereas the trough of the ITD
the CD occurred at minimal discharge (see Figure functions across frequency align at the same ITD for
7–15F). Note that for these idealized neurons, the the LSO neuron. Also, like the model neurons, the
best delay measured from the composite curves (see CP for the MSO neuron is near 0 cycles whereas that
Figures 7–15B and 7–15E) matches the CD. for the LSO neuron is near 0.5 cycles, and in both
The ITD sensitivity of actual MSO and LSO neu- cases the CD is similar to the best delay.
rons are remarkably similar to the idealized model The representation of ITDs and the neural code
neurons depicted in Figures 7–14 and 7–15. Figure for locating a low-frequency sound source along the
7–16 displays the ITD properties of a MSO and LSO azimuth is a subject of considerable debate (Joris
Figure 7–16. Responses of a MSO, peak-type (A–C) and a LSO, trough-type (D–F) neuron. A and D. ITD functions across
frequency for the MSO peak and MSO neuron, respectively. B and E. Composite curve derived from averaging the func-
tions in A and D. C and F. Linear fit of mean interaural phase versus stimulus frequency for the MSO and LSO neuron.
Characteristic phase (CP) is the phase intercept at 0 Hz and the characteristic delay (CD) is the slope of the linear fit. Panel
A adapted from Yin and Chan (1990), with permission of The American Physiological Society.
& Yin, 2007). The classic view proposed in 1948 by would be inoperative due to the sparseness of the
Lloyd Jeffress (1948) postulated an array of coinci- ITD array. In contrast, for a medium (e.g., cat, ±400
dence detectors (e.g., MSO neurons) each with its µsec) or large size head (e.g., human, ±825 µsec), the
own set of neural delay lines from each ear that off- medial slope only constitute a small part of the natu-
set the acoustic delays created between the ears from ral ITD range. So, a Jeffress-type place code would
a sound source along the azimuthal plane. In this be optimal and ITD created by a sound source would
way an ITD code could be transformed into a place create focused neural activity in the ITD/azimuthal
code for sound localization. Many of the anatomic plane. In the middle panel of Figure 7–17, the width
(Beckius et al., 1999; Smith et al., 1993) and physi- of the ITD functions have been broadened. This situ-
ologic features of the MSO and its inputs have been ation allows the count comparison model to operate
found to be consistent with the Jeffress model (Batra for both small and medium head size and a sparse
et al., 1997; Goldberg & Brown, 1969; Spitzer & Sem- array for animals with a large head size. In the bot-
ple, 1995; Yin & Chan, 1990; ). However, the finding tom panel, the width of the ITD functions have been
that the best ITD of a neuron was related to its best broadened even more and here the count compari-
frequency and that the peaks of the ITD functions son model operates over a broad range of head sizes.
for small-headed animals were often outside of the In summary, when the ITD functions are narrow and
range that such animals would normally encoun- dense (see Figure 7–17, upper panel), the count com-
ter (McAlpine et al., 2001) led to a resurrection of parison model only operates for small head sizes. As
the count comparison model first proposed by von the ITD functions broaden and become sparse, the
Békésy (1930) and van Bergeijk (1962) that sound count comparison model can encompass large and
localization could be achieved by comparing activ- larger head sizes. However, the amount of broad-
ity in a structure on one side of the brain with the ening needed to make the count comparison model
activity of the equivalent structure on the other side. work for all head sizes and all frequencies exceeds
McAlpine et al.(2001) noted that the medial slope the physiological evidence (Palmer & Kuwada,
of the ITD functions, independent of the neuron’s 2005). Harper and McAlpine, (2004) concluded that
best frequency, fell within the physiological range a count comparison mechanism may operate for
of small-headed animals and changes in ITD would small-headed animals and a Jeffress place model for
create rapid changes in response rate (also see Skot- large-headed animals.
tun et al., 2001). Brand et al. (2002) and Pecka et al.
(2008) provided evidence in the MSO of gerbils that
inhibitory mechanisms could shift the peaks of the Processing of ILDs
ITD functions outward so that the steep part of this
function is always within the physiologic range of Although the data presented above argue for a
the animal. weak role of LSO cells in coding ITDs of complex
A schema comparing the Jeffress place code stimuli, the basic IE response property of LSO cells
model with slope, count comparison model is pre- has traditionally been considered to convey a role
sented in Figure 7–17. The upper panel depicts an in ILD processing (Boudreau & Tsuchitani, 1970).
array of ITD-sensitive neurons, each tuned to a par- As discussed above, LSO cells receive excitatory
ticular ITD. Also shown at the top is the range of inputs from the ipsilateral CN and inhibitory inputs
ITDs encountered by animals with different head relayed by glycinergic neurons of the MNTB that are
sizes. For animals with a small head size (e.g., gerbil, in turn excited by the calyces of Held synapses from
±125 µsec), the array is limited and only the medial globular bushy cells of the contralateral CN. The end
slopes (heavy blue and red lines) fall within the result is that LSO cells are excited by stimulation of
natural range. In this case, the ITD created by a the ipsilateral ear and inhibited by stimulation of the
sound source, depending on its location, would cre- contralateral ear. In this way they are sensitive to the
ate activity on one side of the brain that could be ILD at the two ears. Usually, this has been studied
compared with the activity on the opposite side of using dichotic stimuli so that the inputs to each ear
the brain. In this example, the Jeffress place code can be precisely specified.
Figure 7–17. Schematic of two models of sound localization. Displayed is an array of ITD-sensitive neurons, each tuned
to a particular ITD. The extent of the array depends on the size of the head and in our schematic is shown for ±100 µsec
(e.g., gerbil), ±400 µsec (e.g., cat), and ±800 µsec (e.g., humans). The heavy lines centered about an ITD of 0 µsec are the func-
tions used in a slope, count comparison model whereas the entire array are the functions used in a peak-picking or Jeffress
model. Top panel: Half-width of ITD functions is 200 µsec; for the middle panel, 800 µsec; and for the bottom panel, 1600 µsec.
180
Figure 7–18 shows responses of an LSO cell the shape of the receptive field is determined by the
illustrating its sensitivity to ILDs. Figures 7–18A cell’s ILD sensitivity. Taking advantage of the virtual
through 7–18D show the dot rasters and associated space technique, Tollin and Yin ( 2002b) systemati-
histograms of responses to 300 ms duration best fre- cally manipulated the three spatial localization cues
quency tones (16 kHz) with the ipsilateral excitatory of ITDs, ILDs and spectral cues to see which cue was
tone held at 30 dB SPL while the contralateral tone most important in the shape of the receptive field.
is raised from 5 dB SPL (see Figure 7–18A) to 45 dB Figure 7–19 shows an example of the manipula-
SPL (see Figure 7–18D). By holding the excitatory tions in one LSO neuron. The idea is to vary only
ipsilateral stimulus constant, the inhibitory effect of one of the cues while holding the other two cues
the contralateral input is clearly seen as it is raised constant. For example, Figure 7–19A shows results
in level. The spike count is plotted as a function of that explore the potency of the ITD cue. The curve
ILD (defined as the contralateral level in dB minus labeled “Normal” shows the receptive field of the
the ipsilateral level) in Figure 7–18E. Negative ILDs neuron when all three cues are varied naturally, that
correspond to higher levels to the ipsilateral ear. ILD is, it shows the receptive field of the cell. The curves
sensitivity can be quantified by the half-maximal labeled Δ-ITD shows responses when the other two
ILD, which designates the ILD at which the response cues were held constant at values corresponding to
is half-maximal, and the slope of the function. In Fig- the point straight ahead (ILD = 0 and spectral cues
ure 7–18E the half-maximal ILD is about -6 dB. In of the straight-ahead position) but ITDs were var-
general, different cells will have different half-max- ied from those values corresponding to -90 deg in
imal ILDs, thereby covering the range of possible the ipsilateral field to +90 deg in the contralateral
ILDs occurring in natural conditions. There are a field. The nearly flat line suggests that ITDs by them-
few reports of systematic topographical representa- selves do not modulate the cell’s response. This is
tion of half-maximal ILDs across one dimension of a reinforced by the responses in the “0-ITD” condi-
nucleus: cells in the deep and intermediate layers of tion, where the ITDs were held at 0 and the ILDs and
the superior colliculus (Wise & Irvine, 1985) and in spectral cues varied normally. The close correspon-
the 60 kHz region of the bat IC (Park & Pollak, 1994). dence of the “Normal” and “0-ITD” curves again
Surprisingly, there are no reports of the receptive suggest that ITDs are not important parameters in
field properties of LSO using free-field stimuli. Tollin determining the receptive field response.
and Yin ( 2002a) studied the receptive field properties Figure 7–19B shows analogous manipulations
of LSO using virtual space techniques by delivering of the spectral cues and the responses are similar to
the stimuli dichotically but filtering the broad band those in Figure 7–19A. These suggest that spectral
noise by the HRTFs of the cat to simulate sounds at cues are also not critical in the normal receptive field
different spatial locations. As expected from the IE sensitivity of the cell.
binaural property of LSO cells, the spatial receptive Figure 7–19C shows contrasting results when
fields of LSO neurons had peaks in the ipsilateral ILDs are studied. In this case the “Normal” and
sound field where the excitatory ipsilateral input “Δ-ILD” responses are nearly identical, suggesting
would be dominant and decreased responses in the that ILDs are the key determinant in the normal
contralateral field. That the response in the contra- receptive field response. This is confirmed by the flat
lateral sound field arose from the inhibition from the response in the “0-ILD” curve which shows that the
contralateral ear was demonstrated by turning off the cell is not modulated by normal variations in ITDs
input to the contralateral ear (Figure 7–19D), a trivial and spectral cues when ILDs are held at 0. While dif-
procedure using virtual space stimuli but much more ferent LSO cells showed different degrees of modu-
difficult to do in free field. lation with the cue manipulation paradigms shown
Because ILDs are an inherent component of in Figure 7–19, for the most part similar responses
free-field sound stimuli, vary in a systematic fashion were found for all 24 LSO neurons studied. Thus, in
for stimuli in different spatial locations (see Figure accordance with the classical view, ILDs are by far
7–11), and strongly modulate the responses of LSO the most important factor in shaping the receptive
neurons (see Figure 7–18), it is natural to think that field profile for most LSO neurons.

182
Figure 7–18. Responses of an LSO cell to variations in the ILD of a CF tone. A through D, Dot rasters and PST histograms in response to a 300-msec ipsilateral
tone at 30 dB SPL as a function of the level of a tone at the contralateral ear, as shown in the top right of each panel. The inset in A shows the first 40 msec of the
response to short tone pips at CF presented monaurally to the ipsilateral ear only, demonstrating the characteristic chopping response exhibited by most of our cells
(bin width, 400 μsec and the top tic on the ordinate, 150 spikes). E. Mean discharge rate ±1 SEM versus ILD (in decibels: SPL). (In this and all subsequent figures,
where the error bars are not present, the SEM is less than the height of the data point.) The top abscissa indicates the level of the tone at the contralateral ear, and
the right ordinate shows the rate normalized to the maximum. The dashed horizontal line shows the spontaneous rate of the unit. Reproduced from Tollin and Yin
(2002a) with permission by the Society for Neuroscience via Copyright Clearance Center.
Figure 7–19. Spatial receptive fields in azimuth for an LSO cell (CF = 7.8 kHz) to cue manipulations
of the HRTFs. In all graphs the “Normal” (filled circles) response is that recorded with all localization
cues varied naturally. A. ITD manipulations. Responses obtained when the ITD cue was varied normally
(∆-ITD) while ILD and spectra were kept constant are shown by filled squares, where as responses when
the ITD cue was held constant (0-ITD) are shown by open circles. B. Spectral manipulations. Analogous
manipulations as in A except the spectral cue was manipulated. C. ILD manipulations. Same as in A
except ILD was manipulated. D. Comparison of the “normal” and ipsilateral stimulus alone responses.
Reproduced from Tollin and Yin (2002b) with permission by the Society for Neuroscience via Copyright
Clearance Center.
As LSO is involved in processing predomi- et al., 2003; Moore, 2000; Richter et al., 1983), which
nantly high-frequency sounds and the human audi- casts doubt on the importance of the ILD circuit in
tory system is chiefly low frequency, a legitimate the human system (Schwartz, 1992).
question is the relative role of the LSO for human
hearing. Anatomical, postmortem studies of the
Question 2
human SOC have generally acknowledged the exis-
tence of an LSO although diminished relative to the
size of the MSO (Bazwinsky et al., 2003; Moore, 1987; Is it known how the SOC encodes sound
Strominger, 1978). On the other hand, the existence when a patient wears a cochlear implant or
of the MNTB has been controversial (Bazwinsky brainstem implant?
Answer 2 References
There are no studies examining the response
of SOC neurons to cochlear implant stimula- Abou-Madi, L., Pontarotti, P., Tramu, G., Cupo, A., & Eybalin,
tion. However, there are numerous studies M. (1987). Coexistence of putative neuroactive substances
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7

The Superior Olivary Complex

fibers from the cochlea. As both cochlear nuclei

(SPON) although they are not entirely equivalent in

Feedback System to the Cochlea

Our treatment of this system is brief because it is

Figure 7–8. Examples of SOC neurons that show an off

a low-pass shape. When measured as a function of

divergence of the left and right ear traces as a func-

dreau & Tsuchitani, 1970). As expected, the recep-

In order for a neuron to encode ITDs, the inputs from

Created from ufrnbr on 2020-07-20 19:30:22.

iology, 77, 2083–2097.

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